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Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes

BACKGROUND: Transposable elements (TE) have attracted much attention since they shape the genome and contribute to species evolution. Organisms have evolved mechanisms to control TE activity. Testis expressed 19 (Tex19) represses TE expression in mouse testis and placenta. In the human and mouse gen...

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Autores principales: Bianchetti, Laurent, Tarabay, Yara, Lecompte, Odile, Stote, Roland, Poch, Olivier, Dejaegere, Annick, Viville, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4603632/
https://www.ncbi.nlm.nih.gov/pubmed/26459560
http://dx.doi.org/10.1186/s12862-015-0506-y
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author Bianchetti, Laurent
Tarabay, Yara
Lecompte, Odile
Stote, Roland
Poch, Olivier
Dejaegere, Annick
Viville, Stéphane
author_facet Bianchetti, Laurent
Tarabay, Yara
Lecompte, Odile
Stote, Roland
Poch, Olivier
Dejaegere, Annick
Viville, Stéphane
author_sort Bianchetti, Laurent
collection PubMed
description BACKGROUND: Transposable elements (TE) have attracted much attention since they shape the genome and contribute to species evolution. Organisms have evolved mechanisms to control TE activity. Testis expressed 19 (Tex19) represses TE expression in mouse testis and placenta. In the human and mouse genomes, Tex19 and Secreted and transmembrane 1 (Sectm1) are neighbors but are not homologs. Sectm1 is involved in immunity and its molecular phylogeny is unknown. METHODS: Using multiple alignments of complete protein sequences (MACS), we inferred Tex19 and Sectm1 molecular phylogenies. Protein conserved regions were identified and folds were predicted. Finally, expression patterns were studied across tissues and species using RNA-seq public data and RT-PCR. RESULTS: We present 2 high quality alignments of 58 Tex19 and 58 Sectm1 protein sequences from 48 organisms. First, both genes are eutherian-specific, i.e., exclusively present in mammals except monotremes (platypus) and marsupials. Second, Tex19 and Sectm1 have both duplicated in Sciurognathi and Bovidae while they have remained as single copy genes in all further placental mammals. Phylogenetic concordance between both genes was significant (p-value < 0.05) and supported co-evolution and functional relationship. At the protein level, Tex19 exhibits 3 conserved regions and 4 invariant cysteines. In particular, a CXXC motif is present in the N-terminal conserved region. Sectm1 exhibits 2 invariant cysteines and an Ig-like domain. Strikingly, Tex19 C-terminal conserved region was lost in Haplorrhini primates while a Sectm1 C-terminal extra domain was acquired. Finally, we have determined that Tex19 and Sectm1 expression levels anti-correlate across the testis of several primates (ρ = −0.72) which supports anti-regulation. CONCLUSIONS: Tex19 and Sectm1 co-evolution and anti-regulated expressions support a strong functional relationship between both genes. Since Tex19 operates a control on TE and Sectm1 plays a role in immunity, Tex19 might suppress an immune response directed against cells that show TE activity in eutherian reproductive tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0506-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-46036322015-10-14 Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes Bianchetti, Laurent Tarabay, Yara Lecompte, Odile Stote, Roland Poch, Olivier Dejaegere, Annick Viville, Stéphane BMC Evol Biol Research Article BACKGROUND: Transposable elements (TE) have attracted much attention since they shape the genome and contribute to species evolution. Organisms have evolved mechanisms to control TE activity. Testis expressed 19 (Tex19) represses TE expression in mouse testis and placenta. In the human and mouse genomes, Tex19 and Secreted and transmembrane 1 (Sectm1) are neighbors but are not homologs. Sectm1 is involved in immunity and its molecular phylogeny is unknown. METHODS: Using multiple alignments of complete protein sequences (MACS), we inferred Tex19 and Sectm1 molecular phylogenies. Protein conserved regions were identified and folds were predicted. Finally, expression patterns were studied across tissues and species using RNA-seq public data and RT-PCR. RESULTS: We present 2 high quality alignments of 58 Tex19 and 58 Sectm1 protein sequences from 48 organisms. First, both genes are eutherian-specific, i.e., exclusively present in mammals except monotremes (platypus) and marsupials. Second, Tex19 and Sectm1 have both duplicated in Sciurognathi and Bovidae while they have remained as single copy genes in all further placental mammals. Phylogenetic concordance between both genes was significant (p-value < 0.05) and supported co-evolution and functional relationship. At the protein level, Tex19 exhibits 3 conserved regions and 4 invariant cysteines. In particular, a CXXC motif is present in the N-terminal conserved region. Sectm1 exhibits 2 invariant cysteines and an Ig-like domain. Strikingly, Tex19 C-terminal conserved region was lost in Haplorrhini primates while a Sectm1 C-terminal extra domain was acquired. Finally, we have determined that Tex19 and Sectm1 expression levels anti-correlate across the testis of several primates (ρ = −0.72) which supports anti-regulation. CONCLUSIONS: Tex19 and Sectm1 co-evolution and anti-regulated expressions support a strong functional relationship between both genes. Since Tex19 operates a control on TE and Sectm1 plays a role in immunity, Tex19 might suppress an immune response directed against cells that show TE activity in eutherian reproductive tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0506-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-10-12 /pmc/articles/PMC4603632/ /pubmed/26459560 http://dx.doi.org/10.1186/s12862-015-0506-y Text en © Bianchetti et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Bianchetti, Laurent
Tarabay, Yara
Lecompte, Odile
Stote, Roland
Poch, Olivier
Dejaegere, Annick
Viville, Stéphane
Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title_full Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title_fullStr Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title_full_unstemmed Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title_short Tex19 and Sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
title_sort tex19 and sectm1 concordant molecular phylogenies support co-evolution of both eutherian-specific genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4603632/
https://www.ncbi.nlm.nih.gov/pubmed/26459560
http://dx.doi.org/10.1186/s12862-015-0506-y
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