Molecular Signatures Discriminating the Male and the Female Sexual Pathways in the Pearl Oyster Pinctada margaritifera

Type Article
Date 2015-03
Language English
Author(s) Teaniniuraitemoana Vaihiti1, Huvet ArnaudORCID2, Levy Peva1, Gaertner-Mazouni Nabila3, Gueguen YannickORCID1, 4, Le Moullac GillesORCID1
Affiliation(s) 1 : IFREMER, UMR Ecosyst Insulaires Oceaniens EIO 241, Labex Corail, Ctr Pacifique, Taravao 98719, Tahiti, Fr Polynesia.
2 : IFREMER, UMR Lab Sci Environm Marin LEMAR 6539, F-29280 Plouzane, France.
3 : Univ Polynesie Francaise, UMR Ecosyst Insulaires Oceaniens EIO 241, Labex Corail, Faaa 98702, Tahiti, Fr Polynesia.
4 : Univ Montpellier, IFREMER, UMR Ecol Syst Marins Cotiers ECOSYM 5119, Labex Corail, F-34095 Montpellier 5, France.
Source Plos One (1932-6203) (Public Library Science), 2015-03 , Vol. 10 , N. 3 , P. e0122819
DOI 10.1371/journal.pone.0122819
WOS© Times Cited 19
Note Supporting Information : S1 Table. Primer sequences. doi:10.1371/journal.pone.0122819.s001 (XLSX)
Abstract The genomics of economically important marine bivalves is studied to provide better understanding of the molecular mechanisms underlying their different reproductive strategies. The recently available gonad transcriptome of the black-lip pearl oyster Pinctada margaritifera is a novel and powerful resource to study these mechanisms in marine mollusks displaying hermaphroditic features. In this study, RNAseq quantification data of the P. margaritifera gonad transcriptome were analyzed to identify candidate genes in histologically-characterized gonad samples to provide molecular signatures of the female and male sexual pathway in this pearl oyster. Based on the RNAseq data set, stringent expression analysis identified 1,937 contigs that were differentially expressed between the gonad histological categories. From the hierarchical clustering analysis, a new reproduction model is proposed, based on a dual histo-molecular analytical approach. Nine candidate genes were identified as markers of the sexual pathway: 7 for the female pathway and 2 for the male one. Their mRNA levels were assayed by real-time PCR on a new set of gonadic samples. A clustering method revealed four principal expression patterns based on the relative gene expression ratio. A multivariate regression tree realized on these new samples and validated on the previously analyzed RNAseq samples showed that the sexual pathway of P. margaritifera can be predicted by a 3-gene-pair expression ratio model of 4 different genes: pmarg-43476, pmarg-foxl2, pmarg-54338 and pmarg-fem1-like. This 3-gene-pair expression ratio model strongly suggests only the implication of pmarg-foxl2 and pmarg-fem1-like in the sex inversion of P. margaritifera. This work provides the first histo-molecular model of P. margaritifera reproduction and a gene expression signature of its sexual pathway discriminating the male and female pathways. These represent useful tools for understanding and studying sex inversion, sex differentiation and sex determinism in this species and other related species for aquaculture purposes such as genetic selection programs.
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