DNA methylation differences between male and female gonads of the oyster reveal the role of epigenetics in sex determination

Sun, Dongfang; Li, Qi; Yu, Hong

doi:10.1016/j.gene.2022.146260

Cited by 22 publications

(14 citation statements)

References 48 publications

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“…Features of animal age, sex, and reproductive history could also influence the gene expression pattern. Sexually dimorphic gene expression and epigenomic patterns have been identified in a wide variety of species, including octopus [ 76 ], oysters [ 77 ], and tunicates [ 78 ]. Therefore, the sex of the octopus used in this study could be a contributing factor to the gene expression patterns that we uncovered.…”

Section: Discussionmentioning

confidence: 99%

Epigenetic machinery is functionally conserved in cephalopods

2022

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Background Epigenetic regulatory mechanisms are divergent across the animal kingdom, yet these mechanisms are not well studied in non-model organisms. Unique features of cephalopods make them attractive for investigating behavioral, sensory, developmental, and regenerative processes, and recent studies have elucidated novel features of genome organization and gene and transposon regulation in these animals. However, it is not known how epigenetics regulates these interesting cephalopod features. We combined bioinformatic and molecular analysis of Octopus bimaculoides to investigate the presence and pattern of DNA methylation and examined the presence of DNA methylation and 3 histone post-translational modifications across tissues of three cephalopod species. Results We report a dynamic expression profile of the genes encoding conserved epigenetic regulators, including DNA methylation maintenance factors in octopus tissues. Levels of 5-methyl-cytosine in multiple tissues of octopus, squid, and bobtail squid were lower compared to vertebrates. Whole genome bisulfite sequencing of two regions of the brain and reduced representation bisulfite sequencing from a hatchling of O. bimaculoides revealed that less than 10% of CpGs are methylated in all samples, with a distinct pattern of 5-methyl-cytosine genome distribution characterized by enrichment in the bodies of a subset of 14,000 genes and absence from transposons. Hypermethylated genes have distinct functions and, strikingly, many showed similar expression levels across tissues while hypomethylated genes were silenced or expressed at low levels. Histone marks H3K27me3, H3K9me3, and H3K4me3 were detected at different levels across tissues of all species. Conclusions Our results show that the DNA methylation and histone modification epigenetic machinery is conserved in cephalopods, and that, in octopus, 5-methyl-cytosine does not decorate transposable elements, but is enriched on the gene bodies of highly expressed genes and could cooperate with the histone code to regulate tissue-specific gene expression.

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Section: Discussionmentioning

confidence: 99%

Epigenetic machinery is functionally conserved in cephalopods

2022

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“…Sex differences in the genetics between males and females has been reported in many aquaculture species in the form of sex-specific markers [13,21,34] or sex-specific gene expression [18,19,24,35]. However, epigenetic difference between sexes have rarely been reported [7]. In this study, DNA methylation-sensitive RAD (MethylRAD) sequencing was conducted to generate the first large-scale, single-base resolution methylomes for male and female Pseudobagrus ussuriensis.…”

Section: Discussionmentioning

confidence: 99%

“…Besides, high temperature-induced masculinization was also found in Nile tilapia (Oreochromis niloticus) and both female and male tilapia showed an increase in DNA methylation across the whole genome level after high temperature induction [6]. In genetic sex determination (GSD) species, promoter methylation in diacylglycerol kinase delta gene (Dgkd) has been found to be involved in Pacific oyster (Crassostrea gigas) sex determination [7]. Sry gene has been found to play a key role in mammal sex determination and its hypomethylation had been reported to promote testis development [8].…”

Section: Introductionmentioning

confidence: 99%

“…However, there are only a few studies available on the sex difference between male and female samples in epigenetics in aquaculture species. In Pacific oyster (Crassostrea gigas), a whole genome methylation analysis was carried out on female and male gonads which showed a higher level of DNA methylation in male gonads compared with female ones [7]. In tiger pufferfish, 3173 differentially methylated regions (DMRs) were identified between males and females while several differentially methylated genes (DMGs) were also found [20].…”

Section: Introductionmentioning

confidence: 99%

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DNA Methylation Difference between Female and Male Ussuri Catfish (Pseudobagrus ussuriensis) in Brain and Gonad Tissues

Chen

Zhu

et al. 2022

Life

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DNA methylation has been found to be involved in sex determination and differentiation in many aquaculture species. The Ussuri catfish (Pseudobagrus ussuriensis) is a popular aquaculture fish in China with high economic value in which male-biased sex dimorphism was observed in terms of body size and body weight. In this study, DNA methylation-sensitive RAD sequencing (Methyl-RAD) was used to explore the epigenetic difference between adult male and female samples in brain and gonad tissues. In brain tissues, 5,442,496 methylated cytosine sites were found and 9.94% of these sites were from symmetric CCGG or CCWGG sites. Among these sites, 321 differential DNA methylation sites (DMSs) in 171 genes were identified, while in gonad tissues, 4,043,053 methylated cytosines sites were found in total and 11.70% of them were from CCGG or CCWGG. Among these sites, 78 differential DNA methylation sites were found which were located in 64 genes. We also found several sex-determination genes among these differential methylated genes, such as amh, gsdf and hsd11b2 in brain tissues and slco3a1, socs2 and trim47 in gonad tissues. These results provided evidence for understanding the function of DNA methylation in the sex differentiation in Pseudobagrus ussuriensis, which further deepens the relationship between gene regulation and epigenetics.

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“…The gender of parent cohort was determined by checking germ cells during the breeding process. Because progenies were out of sexual maturity stages, offspring samples were sexed by DNA methylation markers at the diacylglycerol kinase delta (DGKD) locus, which was hypermethylated in males and hypomethylated in females [31]. The DNA methylation marker was reconfirmed in parent groups and public data (S2A Fig) . All triploid and two diploid samples were found to be females, while the other four diploid oysters were males (S2B Fig and S2 Table ).…”

Section: Dna Methylation Inheritance and Sex-specific Dna Methylation...mentioning

confidence: 99%

Intergenerational transfer and sex differences of DNA methylation patterns in the Pacific oyster (Crassostrea gigas)

Teng

et al. 2022

Preprint

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Apart from DNA-sequence-based inheritance, inheritance of epigenetic marks such as DNA methylation is controversial across the tree of life. In mammals, post-fertilization and primordial germ cell reprogramming processes erased most parental DNA methylation information. In nonmammalian vertebrates and insects, it has been proposed that DNA methylation is an essential hereditary carrier. However, how and to what extent general DNA methylation reprogramming affects intergenerational inheritance in molluscs remains unclear. Here, we investigated genome-wide DNA methylation in a mollusc model, the Pacific oyster (Crassostrea gigas), to test how epigenetic information transfers from parents to offspring. Analysis of global methylome revealed that the DNA methylation patterns are highly conserved within families. Almost half of the differentially methylated CpG dinucleotides (DMCs) between families in parents could transfer to offspring. These results provided the direct evidence for the hypothesis that the Pacific oyster DNA methylation patterns are inherited in generations. Moreover, distinct DNA methylation differences between male and female somatic tissues in C. gigas are revealed in this study. These sex-differential methylated genes significantly enriched in the regulation of Rho protein signal transduction process, which indicated that DNA methylation might have an essential role in the sexual differentiation of somatic tissues in C. gigas.

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DNA methylation differences between male and female gonads of the oyster reveal the role of epigenetics in sex determination

Cited by 22 publications

References 48 publications

Epigenetic machinery is functionally conserved in cephalopods

Epigenetic machinery is functionally conserved in cephalopods

DNA Methylation Difference between Female and Male Ussuri Catfish (Pseudobagrus ussuriensis) in Brain and Gonad Tissues

Intergenerational transfer and sex differences of DNA methylation patterns in the Pacific oyster (Crassostrea gigas)

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