Genome-Wide Differential DNA Methylomes Provide Insights into the Infertility of Triploid Oysters.

Abstract

Chromosomal incompatibility and gene expression changes would affect the development of polyploid gonad and gamete formation. The role of epigenetics like DNA methylation in reproductive development is fully demonstrated in diploid animals. The lack of polyploid species and the infertility of polyploid animals, especially the odd ploidy, limit the study of epigenetic regulation mechanism of polyploid reproduction. Fertile and infertile individuals exist in triploid Pacific oyster Crassostrea gigas, which provide an interesting model for studies on the effect of epigenetic regulation on gonadal development. The whole genome single base resolution DNA methylomes in gonads of triploid females α (F-3nα), triploid females β (F-3nβ), triploid males α (M-3nα), triploid hermaphrodite predominantly males (HPM-3n), diploid females (F-2n), and diploid males (M-2n) were generated by using bisulfite-sequencing. The overall DNA methylation profiles in gene regions and transposable regions of fertile and infertile triploid oysters were consistent with those of diploid oysters. The DNA methylation level of CG context decreased in infertile triploid oysters, with more hypomethylated than hypermethylated regions, and the opposite is true in fertile triploid oysters. Genes harbored with differentially methylated regions (DMRs) in infertile triploids were mainly related to the metabolism pathways and the signal pathways. Correlation analysis indicated that the expression of gene transcriptions was generally positively associated with DNA methylation in gene body regions, and DMRs in infertile triploid oysters played significant roles in gonadal development as a possible critical epigenetic regulator of gonadal development gene transcriptional activity. These findings indicate a potential relationship between DNA methylation variability and gene expression plasticity in newly formed polyploidy. As far as we know, this is the first study revealing the epigenetic regulation of gonadal development in invertebrates based on fertile and infertile models, meanwhile providing a new mentality to explore the regulatory mechanisms of infertility in triploids.