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


Journal

BMC evolutionary biology
ISSN: 1471-2148
Titre abrégé: BMC Evol Biol
Pays: England
ID NLM: 100966975

Informations de publication

Date de publication:
03 07 2019
Historique:
received: 08 02 2019
accepted: 17 06 2019
entrez: 5 7 2019
pubmed: 5 7 2019
medline: 8 10 2019
Statut: epublish

Résumé

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. 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. 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).

Sections du résumé

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).

Identifiants

pubmed: 31269894
doi: 10.1186/s12862-019-1462-8
pii: 10.1186/s12862-019-1462-8
pmc: PMC6609395
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

137

Références

BMC Evol Biol. 2014 Oct 04;14:212
pubmed: 25281000
FEBS Lett. 2003 Dec 18;555(3):533-8
pubmed: 14675769
Mol Hum Reprod. 2008 Mar;14(3):137-42
pubmed: 18256174
Genetics. 2014 Nov;198(3):1291-308
pubmed: 25233988
Biochem Biophys Res Commun. 2004 Nov 12;324(2):547-53
pubmed: 15474461
J Reprod Dev. 2016 Jun 17;62(3):305-10
pubmed: 26971890
Development. 2005 Sep;132(18):4029-39
pubmed: 16093322
BMC Genomics. 2005 May 20;6:76
pubmed: 15907208
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7793-8
pubmed: 15136734
FEBS Lett. 2009 Jun 18;583(12):1957-63
pubmed: 19427864
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6714-9
pubmed: 17428915
J Cell Biol. 1998 Aug 10;142(3):751-61
pubmed: 9700163
Biol Reprod. 1994 Jan;50(1):129-36
pubmed: 8312436
Anim Reprod Sci. 2007 Feb;97(3-4):303-13
pubmed: 16621350
Cell Mol Life Sci. 2017 Feb;74(3):525-541
pubmed: 27497926
Mol Biol Cell. 2004 Mar;15(3):1031-43
pubmed: 14718556
Int J Biol Sci. 2015 Aug 15;11(10):1226-35
pubmed: 26327816
Spermatogenesis. 2012 Jul 1;2(3):158-166
pubmed: 23087835
PLoS One. 2010 Aug 10;5(8):e12072
pubmed: 20711465
BMC Genomics. 2016 May 18;17:368
pubmed: 27189481
Science. 2012 Dec 21;338(6114):1593-9
pubmed: 23258891
Mol Cell. 2007 May 11;26(3):437-48
pubmed: 17499049
J Cell Sci. 2010 Aug 15;123(Pt 16):2763-72
pubmed: 20647369
Mol Reprod Dev. 2004 Jan;67(1):116-26
pubmed: 14648882
Nat Rev Genet. 2013 Nov;14(11):794-806
pubmed: 24136506
Genome Biol Evol. 2015 Apr 24;7(5):1332-48
pubmed: 25912043
Front Biosci (Elite Ed). 2010 Jun 01;2:841-8
pubmed: 20515757
Genomics. 2007 Feb;89(2):215-23
pubmed: 17049203
Hum Mol Genet. 2003 Jan 15;12(2):169-75
pubmed: 12499397
Curr Top Dev Biol. 2000;50:155-81
pubmed: 10948454
Development. 2014 Oct;141(19):3662-71
pubmed: 25249458
Baillieres Best Pract Res Clin Endocrinol Metab. 2000 Sep;14(3):363-88
pubmed: 11097781
Gen Comp Endocrinol. 2004 Jan 1;135(1):1-16
pubmed: 14644639
Am J Hum Genet. 2012 Nov 2;91(5):958-64
pubmed: 23122589
Biochem Biophys Res Commun. 2016 Sep 16;478(2):592-8
pubmed: 27473657
Genetics. 1999 Apr;151(4):1531-45
pubmed: 10101175
Gene. 2013 Dec 1;531(2):294-300
pubmed: 24055424
Am J Hum Genet. 2013 Aug 8;93(2):336-45
pubmed: 23891469
Philos Trans R Soc Lond B Biol Sci. 2010 May 27;365(1546):1465-80
pubmed: 20403864
Elife. 2017 Sep 25;6:
pubmed: 28945193
Trends Genet. 2003 Nov;19(11):593-7
pubmed: 14585607
BMC Genet. 2016 Feb 29;17:49
pubmed: 26923438
Biol Reprod. 1997 Jun;56(6):1570-5
pubmed: 9166712
Gen Comp Endocrinol. 1998 Feb;109(2):251-8
pubmed: 9473369
J Cell Biol. 2011 Mar 7;192(5):781-95
pubmed: 21383078
Animal. 2018 Jun;12(6):1232-1241
pubmed: 29065946
Dev Cell. 2012 May 15;22(5):1041-51
pubmed: 22595675
Reprod Nutr Dev. 1980;20(1B):241-9
pubmed: 6818628
Am J Hum Genet. 2013 Aug 8;93(2):346-56
pubmed: 23891471
Hum Genet. 2017 May;136(5):637-655
pubmed: 28456834
Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
pubmed: 21768607
Semin Cell Dev Biol. 2018 Jul;79:80-91
pubmed: 29024760
Nat Genet. 1998 Dec;20(4):377-80
pubmed: 9843212
Poult Sci. 1999 Mar;78(3):444-52
pubmed: 10090273
PLoS One. 2013 Sep 10;8(9):e73951
pubmed: 24040125
Biol Reprod. 2018 Sep 1;99(3):565-577
pubmed: 29635430
Genes Cells. 2016 Jul;21(7):728-39
pubmed: 27353389
Genome Biol Evol. 2018 Oct 1;10(10):2629-2642
pubmed: 30060195

Auteurs

Sophie Fouchécourt (S)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France. sophie.fouchecourt@inra.fr.

Floriane Picolo (F)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Sébastien Elis (S)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Charlotte Lécureuil (C)

Institut de Recherche sur la Biologie de l'Insecte (IRBI), UMR 7261, CNRS-Université de Tours, 37200, Tours, France.

Aurore Thélie (A)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Marina Govoroun (M)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Mégane Brégeon (M)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Pascal Papillier (P)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Jean-Jacques Lareyre (JJ)

INRA, UPR 1037, Laboratory of Fish Physiology and Genomics (LPGP), BIOSIT, OUEST-genopole, Bât. 16, Campus de Beaulieu, cedex, 35042, Rennes, France.

Philippe Monget (P)

PRC, CNRS, IFCE, INRA, Université de Tours, 37380, Nouzilly, France.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH