An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse

Abstract Background Previously, we have demonstrated that genes involved in ovarian function are highly conserved throughout evolution. In this study, we aimed to document the conservation of genes involved in spermatogenesis from flies to vertebrates and their expression profiles in vertebrates. Re...

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Main Authors: Sophie Fouchécourt, Floriane Picolo, Sébastien Elis, Charlotte Lécureuil, Aurore Thélie, Marina Govoroun, Mégane Brégeon, Pascal Papillier, Jean-Jacques Lareyre, Philippe Monget
Format: Article
Language:English
Published: BMC 2019-07-01
Series:BMC Evolutionary Biology
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Online Access:http://link.springer.com/article/10.1186/s12862-019-1462-8
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author Sophie Fouchécourt
Floriane Picolo
Sébastien Elis
Charlotte Lécureuil
Aurore Thélie
Marina Govoroun
Mégane Brégeon
Pascal Papillier
Jean-Jacques Lareyre
Philippe Monget
author_facet Sophie Fouchécourt
Floriane Picolo
Sébastien Elis
Charlotte Lécureuil
Aurore Thélie
Marina Govoroun
Mégane Brégeon
Pascal Papillier
Jean-Jacques Lareyre
Philippe Monget
author_sort Sophie Fouchécourt
collection DOAJ
description Abstract Background Previously, we have demonstrated that genes involved in ovarian function are highly conserved throughout evolution. In this study, we aimed to document the conservation of genes involved in spermatogenesis from flies to vertebrates and their expression profiles in vertebrates. Results We retrieved 379 Drosophila melanogaster genes that are functionally involved in male reproduction according to their mutant phenotypes and listed their vertebrate orthologs. 83% of the fly genes have at least one vertebrate ortholog for a total of 625 mouse orthologs. This conservation percentage is almost twice as high as the 42% rate for the whole fly genome and is similar to that previously found for genes preferentially expressed in ovaries. Of the 625 mouse orthologs, we selected 68 mouse genes of interest, 42 of which exhibited a predominant relative expression in testes and 26 were their paralogs. These 68 mouse genes exhibited 144 and 60 orthologs in chicken and zebrafish, respectively, gathered in 28 groups of paralogs. Almost two thirds of the chicken orthologs and half of the zebrafish orthologs exhibited a relative expression ≥50% in testis. Finally, our focus on functional in silico data demonstrated that most of these genes were involved in the germ cell process, primarily in structure elaboration/maintenance and in acid nucleic metabolism. Conclusion Our work confirms that the genes involved in germ cell development are highly conserved across evolution in vertebrates and invertebrates and display a high rate of conservation of preferential testicular expression among vertebrates. Among the genes highlighted in this study, three mouse genes (Lrrc46, Pabpc6 and Pkd2l1) have not previously been described in the testes, neither their zebrafish nor chicken orthologs. The phylogenetic approach developed in this study finally allows considering new testicular genes for further fundamental studies in vertebrates, including model species (mouse and zebrafish).
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spelling doaj.art-cc18ac64cb2b4b8b90034a8c8035db692022-12-21T21:46:04ZengBMCBMC Evolutionary Biology1471-21482019-07-0119111510.1186/s12862-019-1462-8An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouseSophie Fouchécourt0Floriane Picolo1Sébastien Elis2Charlotte Lécureuil3Aurore Thélie4Marina Govoroun5Mégane Brégeon6Pascal Papillier7Jean-Jacques Lareyre8Philippe Monget9PRC, CNRS, IFCE, INRA, Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursPRC, CNRS, IFCE, INRA, Université de ToursINRA, UPR 1037, Laboratory of Fish Physiology and Genomics (LPGP), BIOSIT, OUEST-genopole, Bât. 16, Campus de BeaulieuPRC, CNRS, IFCE, INRA, Université de ToursAbstract Background Previously, we have demonstrated that genes involved in ovarian function are highly conserved throughout evolution. In this study, we aimed to document the conservation of genes involved in spermatogenesis from flies to vertebrates and their expression profiles in vertebrates. Results We retrieved 379 Drosophila melanogaster genes that are functionally involved in male reproduction according to their mutant phenotypes and listed their vertebrate orthologs. 83% of the fly genes have at least one vertebrate ortholog for a total of 625 mouse orthologs. This conservation percentage is almost twice as high as the 42% rate for the whole fly genome and is similar to that previously found for genes preferentially expressed in ovaries. Of the 625 mouse orthologs, we selected 68 mouse genes of interest, 42 of which exhibited a predominant relative expression in testes and 26 were their paralogs. These 68 mouse genes exhibited 144 and 60 orthologs in chicken and zebrafish, respectively, gathered in 28 groups of paralogs. Almost two thirds of the chicken orthologs and half of the zebrafish orthologs exhibited a relative expression ≥50% in testis. Finally, our focus on functional in silico data demonstrated that most of these genes were involved in the germ cell process, primarily in structure elaboration/maintenance and in acid nucleic metabolism. Conclusion Our work confirms that the genes involved in germ cell development are highly conserved across evolution in vertebrates and invertebrates and display a high rate of conservation of preferential testicular expression among vertebrates. Among the genes highlighted in this study, three mouse genes (Lrrc46, Pabpc6 and Pkd2l1) have not previously been described in the testes, neither their zebrafish nor chicken orthologs. The phylogenetic approach developed in this study finally allows considering new testicular genes for further fundamental studies in vertebrates, including model species (mouse and zebrafish).http://link.springer.com/article/10.1186/s12862-019-1462-8Gene evolutionConservationTestisSpermatogenesis
spellingShingle Sophie Fouchécourt
Floriane Picolo
Sébastien Elis
Charlotte Lécureuil
Aurore Thélie
Marina Govoroun
Mégane Brégeon
Pascal Papillier
Jean-Jacques Lareyre
Philippe Monget
An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
BMC Evolutionary Biology
Gene evolution
Conservation
Testis
Spermatogenesis
title An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
title_full An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
title_fullStr An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
title_full_unstemmed An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
title_short An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse
title_sort evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish chicken and mouse
topic Gene evolution
Conservation
Testis
Spermatogenesis
url http://link.springer.com/article/10.1186/s12862-019-1462-8
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