Gonadal transcriptomes associated with sex phenotypes provide potential male and female candidate genes of sex determination or early differentiation in Crassostrea gigas, a sequential hermaphrodite mollusc

Type Article
Date 2021-08
Language English
Author(s) Broquard Coralie1, 2, 3, Saowaros Suwansa-Ard4, 5, Lepoittevin Mélanie1, 2, Degremont LionelORCID3, Lamy Jean-BaptisteORCID3, Morga BenjaminORCID3, Elizur Abigail, Martinez Anne-SophieORCID1, 2, 5
Affiliation(s) 1 : Normandie University, UNICAEN, CNRS, BOREA, 14000, Caen, France
2 : Laboratoire de Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie, MNHN, SU, UA, CNRS, IRD, Esplanade de la Paix, CS 14032, 14032, Cedex 05, Caen, France
3 : Ifremer, RBE-SG2M-LGPMM, La Tremblade, France
4 : Department of Anatomy, Faculty of Science, Mahidol University, Bangkok, Thailand
5 : Genecology Research Centre, University of the Sunshine Coast, Sippy Downs, Queensland, Australia
Source Bmc Genomics (1471-2164) (Springer Science and Business Media LLC), 2021-08 , Vol. 22 , N. 1 , P. 609 (16p.)
DOI 10.1186/s12864-021-07838-1
WOS© Times Cited 4
Keyword(s) RNA-Seq, Gonad transcriptome, Early sex differentiation, Sex determination, Irregular hermaphrodite, Oyster
Abstract

Background

In the animal kingdom, mollusca is an important phylum of the Lophotrochozoa. However, few studies have investigated the molecular cascade of sex determination/early gonadal differentiation within this phylum. The oyster Crassostrea gigas is a sequential irregular hermaphrodite mollusc of economic, physiological and phylogenetic importance. Although some studies identified genes of its sex-determining/−differentiating pathway, this particular topic remains to be further deepened, in particular with regard to the expression patterns. Indeed, these patterns need to cover the entire period of sex lability and have to be associated to future sex phenotypes, usually impossible to establish in this sequential hermaphrodite. This is why we performed a gonadal RNA-Seq analysis of diploid male and female oysters that have not changed sex for 4 years, sampled during the entire time-window of sex determination/early sex differentiation (stages 0 and 3 of the gametogenetic cycle). This individual long-term monitoring gave us the opportunity to explain the molecular expression patterns in the light of the most statistically likely future sex of each oyster.

Results

The differential gene expression analysis of gonadal transcriptomes revealed that 9723 genes were differentially expressed between gametogenetic stages, and 141 between sexes (98 and 43 genes highly expressed in females and males, respectively). Eighty-four genes were both stage- and sex-specific, 57 of them being highly expressed at the time of sex determination/early sex differentiation. These 4 novel genes including Trophoblast glycoprotein-like, Protein PML-like, Protein singed-like and PREDICTED: paramyosin, while being supported by RT-qPCR, displayed sexually dimorphic gene expression patterns.

Conclusions

This gonadal transcriptome analysis, the first one associated with sex phenotypes in C. gigas, revealed 57 genes highly expressed in stage 0 or 3 of gametogenesis and which could be linked to the future sex of the individuals. While further study will be needed to suggest a role for these factors, some could certainly be original potential actors involved in sex determination/early sex differentiation, like paramyosin and could be used to predict the future sex of oysters.

Full Text
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Publisher's official version 16 2 MB Open access
Additional file 1 Eighty-four genes identified in the C. gigas transcriptome by RNA-Seq Differential gene Expression Analysis (DEA): Name, NCBI gene ID, fold change (male vs female), p-value, FDR ... 19 KB Open access
Additional file 2 Statistical bilateral Wilcoxon tests performed for RT-qPCR experiments at each gametogenetic stage between sexes. Significance at p < 0.05. 1 391 KB Open access
Additional file 3. Primers used for RT-qPCR: list, sequences, number of bases, blasted name of the gene amplified, R2 and % of PCR efficiency. 11 KB Open access
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How to cite 

Broquard Coralie, Saowaros Suwansa-Ard, Lepoittevin Mélanie, Degremont Lionel, Lamy Jean-Baptiste, Morga Benjamin, Elizur Abigail, Martinez Anne-Sophie (2021). Gonadal transcriptomes associated with sex phenotypes provide potential male and female candidate genes of sex determination or early differentiation in Crassostrea gigas, a sequential hermaphrodite mollusc. Bmc Genomics, 22(1), 609 (16p.). Publisher's official version : https://doi.org/10.1186/s12864-021-07838-1 , Open Access version : https://archimer.ifremer.fr/doc/00718/83026/