The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark

Abstract Nanos are RNA-binding proteins playing crucial roles in germ cell development and maintenance. Based on phylogenetic and synteny analyses, this study reveals that nanos1 gene has undergone multiple duplications and gene copies losses in Vertebrates. Chondrichthyan species display two nanos1...

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Main Authors: Laura Gribouval, Pascal Sourdaine, Jean-Jacques Lareyre, Johanna Bellaiche, Florence Le Gac, Sylvie Mazan, Cécile Guiardiere, Pierrïck Auvray, Aude Gautier
Format: Article
Language:English
Published: Nature Portfolio 2018-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-24643-1
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author Laura Gribouval
Pascal Sourdaine
Jean-Jacques Lareyre
Johanna Bellaiche
Florence Le Gac
Sylvie Mazan
Cécile Guiardiere
Pierrïck Auvray
Aude Gautier
author_facet Laura Gribouval
Pascal Sourdaine
Jean-Jacques Lareyre
Johanna Bellaiche
Florence Le Gac
Sylvie Mazan
Cécile Guiardiere
Pierrïck Auvray
Aude Gautier
author_sort Laura Gribouval
collection DOAJ
description Abstract Nanos are RNA-binding proteins playing crucial roles in germ cell development and maintenance. Based on phylogenetic and synteny analyses, this study reveals that nanos1 gene has undergone multiple duplications and gene copies losses in Vertebrates. Chondrichthyan species display two nanos1 genes (named nanos1A/1B), which were both retrieved in some Osteichthyes at basal positions in Sarcopterygii and Actinopterygii lineages. In contrast, Teleosts have lost nanos1A but duplicated nanos1B leading to the emergence of two ohnologs (nanos1Ba/1Bb), whereas Tetrapods have lost nanos1B gene. The two successive nanos gene duplications may result from the second and third whole genome duplication events at the basis of Vertebrates and Teleosts respectively. The expression profiles of nanos1A and nanos1B paralogs were characterized in the dogfish, Scyliorhinus canicula. Nanos1A was strongly expressed in brain and also localized in all germ cell types in the polarized testis. In contrast, nanos1B was detected in testis with the highest expression in the germinative zone. In addition, Nanos1B protein was predominantly located in the nuclei of male germinal cells. In the ovary, both paralogs were detected in germinal and somatic cells. Our study opens new perspectives concerning the complex evolution of nanos1 paralogs and their potential distinct roles in Vertebrates gonads.
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spelling doaj.art-0b3fba8400bc40b9bd42de0109f7d5202024-03-24T12:21:30ZengNature PortfolioScientific Reports2045-23222018-05-018111410.1038/s41598-018-24643-1The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a sharkLaura Gribouval0Pascal Sourdaine1Jean-Jacques Lareyre2Johanna Bellaiche3Florence Le Gac4Sylvie Mazan5Cécile Guiardiere6Pierrïck Auvray7Aude Gautier8Normandie University, UNICAEN, Sorbonne Universités, MNHN, UPMC University Paris 06, UA, CNRS, IRD, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), CS14032Normandie University, UNICAEN, Sorbonne Universités, MNHN, UPMC University Paris 06, UA, CNRS, IRD, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), CS14032INRA UPR1037, Laboratory of Fish Physiology and Genomics, BIOSIT, Ouest-GenopoleINRA UPR1037, Laboratory of Fish Physiology and Genomics, BIOSIT, Ouest-GenopoleINRA UPR1037, Laboratory of Fish Physiology and Genomics, BIOSIT, Ouest-GenopoleCNRS-UPMC-Sorbonne Universités, UMR 7232, Observatoire océanologiqueKELIA, Parc Technopolitain Atalante Saint MaloKELIA, Parc Technopolitain Atalante Saint MaloNormandie University, UNICAEN, Sorbonne Universités, MNHN, UPMC University Paris 06, UA, CNRS, IRD, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), CS14032Abstract Nanos are RNA-binding proteins playing crucial roles in germ cell development and maintenance. Based on phylogenetic and synteny analyses, this study reveals that nanos1 gene has undergone multiple duplications and gene copies losses in Vertebrates. Chondrichthyan species display two nanos1 genes (named nanos1A/1B), which were both retrieved in some Osteichthyes at basal positions in Sarcopterygii and Actinopterygii lineages. In contrast, Teleosts have lost nanos1A but duplicated nanos1B leading to the emergence of two ohnologs (nanos1Ba/1Bb), whereas Tetrapods have lost nanos1B gene. The two successive nanos gene duplications may result from the second and third whole genome duplication events at the basis of Vertebrates and Teleosts respectively. The expression profiles of nanos1A and nanos1B paralogs were characterized in the dogfish, Scyliorhinus canicula. Nanos1A was strongly expressed in brain and also localized in all germ cell types in the polarized testis. In contrast, nanos1B was detected in testis with the highest expression in the germinative zone. In addition, Nanos1B protein was predominantly located in the nuclei of male germinal cells. In the ovary, both paralogs were detected in germinal and somatic cells. Our study opens new perspectives concerning the complex evolution of nanos1 paralogs and their potential distinct roles in Vertebrates gonads.https://doi.org/10.1038/s41598-018-24643-1
spellingShingle Laura Gribouval
Pascal Sourdaine
Jean-Jacques Lareyre
Johanna Bellaiche
Florence Le Gac
Sylvie Mazan
Cécile Guiardiere
Pierrïck Auvray
Aude Gautier
The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
Scientific Reports
title The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
title_full The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
title_fullStr The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
title_full_unstemmed The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
title_short The nanos1 gene was duplicated in early Vertebrates and the two paralogs show different gonadal expression profiles in a shark
title_sort nanos1 gene was duplicated in early vertebrates and the two paralogs show different gonadal expression profiles in a shark
url https://doi.org/10.1038/s41598-018-24643-1
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