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Molecular signatures discriminating the male and the female sexual pathways in the pearl oyster Pinctada margaritifera.

Teaniniuraitemoana V, Huvet A, Levy P, Gaertner-Mazouni N, Gueguen Y, Le Moullac G - PLoS ONE (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Ifremer, UMR 241 Ecosystèmes Insulaires Océaniens (EIO), Labex Corail, Centre du Pacifique, BP 7004, 98719 Taravao, Tahiti, French Polynesia.

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.

No MeSH data available.


Related in: MedlinePlus

The histo-molecular model of the reproduction of P. margaritifera.M or F: male or female in gametogenesis; (M/F)E: male/female at early stage; (M/F)I: male/female at intermediate stage; (M/F)M: male/female at mature stage; (M/F)R: male/female at regression stage; Und(M/F): gonad undifferentiated at the cellular level, beginning a male or a female differentiation at the molecular level; Inv(M/F): oyster in sexual inversion female to male or male to female; MRF: male in regression stage at the cellular level beginning a female differentiation at the molecular level; and FRM: female in regression stage at cellular level beginning a male differentiation at the molecular level.
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pone.0122819.g007: The histo-molecular model of the reproduction of P. margaritifera.M or F: male or female in gametogenesis; (M/F)E: male/female at early stage; (M/F)I: male/female at intermediate stage; (M/F)M: male/female at mature stage; (M/F)R: male/female at regression stage; Und(M/F): gonad undifferentiated at the cellular level, beginning a male or a female differentiation at the molecular level; Inv(M/F): oyster in sexual inversion female to male or male to female; MRF: male in regression stage at the cellular level beginning a female differentiation at the molecular level; and FRM: female in regression stage at cellular level beginning a male differentiation at the molecular level.

Mentions: All these results reveal the importance of considering both histological and molecular, approaches in the description and the understanding of the atypical reproduction of P. margaritifera. Indeed, these previous results allow us to propose a kinetic of the gonadic sex and stages found in the male and the female sexual pathway of this species, modeled in Fig. 7.


Molecular signatures discriminating the male and the female sexual pathways in the pearl oyster Pinctada margaritifera.

Teaniniuraitemoana V, Huvet A, Levy P, Gaertner-Mazouni N, Gueguen Y, Le Moullac G - PLoS ONE (2015)

The histo-molecular model of the reproduction of P. margaritifera.M or F: male or female in gametogenesis; (M/F)E: male/female at early stage; (M/F)I: male/female at intermediate stage; (M/F)M: male/female at mature stage; (M/F)R: male/female at regression stage; Und(M/F): gonad undifferentiated at the cellular level, beginning a male or a female differentiation at the molecular level; Inv(M/F): oyster in sexual inversion female to male or male to female; MRF: male in regression stage at the cellular level beginning a female differentiation at the molecular level; and FRM: female in regression stage at cellular level beginning a male differentiation at the molecular level.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4376701&req=5

pone.0122819.g007: The histo-molecular model of the reproduction of P. margaritifera.M or F: male or female in gametogenesis; (M/F)E: male/female at early stage; (M/F)I: male/female at intermediate stage; (M/F)M: male/female at mature stage; (M/F)R: male/female at regression stage; Und(M/F): gonad undifferentiated at the cellular level, beginning a male or a female differentiation at the molecular level; Inv(M/F): oyster in sexual inversion female to male or male to female; MRF: male in regression stage at the cellular level beginning a female differentiation at the molecular level; and FRM: female in regression stage at cellular level beginning a male differentiation at the molecular level.
Mentions: All these results reveal the importance of considering both histological and molecular, approaches in the description and the understanding of the atypical reproduction of P. margaritifera. Indeed, these previous results allow us to propose a kinetic of the gonadic sex and stages found in the male and the female sexual pathway of this species, modeled in Fig. 7.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Ifremer, UMR 241 Ecosystèmes Insulaires Océaniens (EIO), Labex Corail, Centre du Pacifique, BP 7004, 98719 Taravao, Tahiti, French Polynesia.

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.

No MeSH data available.


Related in: MedlinePlus