Genome-wide DNA methylation profiles provide insight into epigenetic regulation of red and white muscle development in Chinese perch Siniperca chuatsi

Pan, Ya–Xiong; Chen, Lin; Cheng, Jia; Zhu, Xin; Wu, Ping; Bao, Lingsheng; Chu, Wuying; He, Shan; Liang, Xu‐Fang; Zhang, Jianshe

doi:10.1016/j.cbpb.2021.110647

Cited by 19 publications

(8 citation statements)

References 54 publications

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“…However, recent research indicates that in some specific genes, the first intron’s methylation is related to gene expression (Anastasiadi et al 2018). In accordance with the present results, the methylation pattern was similar to previous studies on Chinese perch, which showed the most DMR was concentrated in the intronic regions (Pan et al 2021). Meanwhile, intronic enhancers that interact with the promoters of the relevant genes could partially explain it.…”

Section: Discussionsupporting

confidence: 93%

Fertilization by short-term stored sperm alters DNA methylation patterns in common carp (Cyprinus carpio) embryos at single-base resolution

Cheng,

Zhang,

Nayak

et al. 2024

Preprint

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Short-term storage of sperm in vitro is widely used for artificial fertilization in aquaculture. It has been shown that short-term storage affects sperm motility characteristics, resulting in diminished fertility. However, the detrimental effects of short-term sperm storage on embryos development have remained largely unexplored in single-base methylome resolution. The main aim of the present study was to investigate DNA methylation in the offspring of common carp (Cyprinus carpio) derived from short-term stored sperm. Sperm were stored in artificial seminal plasma on ice (0-2°C) for 0, 3 and 6 days in vitro, fertilization was performed using oocytes from a single female, and embryos were collected at the mid-blastula stage. Sperm and embryo DNA was extracted, analysed by liquid chromatography with tandem mass spectrometry (LC-MS/MS) and whole genome bisulfite sequencing (WGBS). DNA methylation was then assessed. Sperm storage showed negative effects on motility, viability and DNA integrity, but had no effect on global DNA methylation of spermatozoa and resulting embryos. Results from the WGBS showed that methylation of 3313 genes was affected in the embryos fertilized with the 6-day-stored sperm, and the differentially methylated regions (DMRs) identified were mainly involved in cell adhesion, calcium, mitogen-activated protein kinase and adrenergic signalling, melanogenesis, metabolism and RNA transport. Such results suggest that prolongation of storage time may have certain impacts on embryonic development. These initial results provide valuable information for future consideration of the DNA methylome in embryos generated from short-term stored sperm, which is widely used for genetic management of broodstock in aquaculture.

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Section: Discussionsupporting

confidence: 93%

Fertilization by short-term stored sperm alters DNA methylation patterns in common carp (Cyprinus carpio) embryos at single-base resolution

Cheng,

Zhang,

Nayak

et al. 2024

Preprint

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“…The overall genome-wide methylation patterns were different between two groups. Our results showed that the cytosine methylation levels under CG context were much higher than those under CHG and CHH contexts, which was consistent with evidence reported in grass carp and other fish species ( Cai et al, 2020 ; Pan et al, 2021 ). Through the analysis of DNA methylation levels across the distinct genomic features and entire transcriptional units, we found that about 80% of CG was methylated in all regions, which is consistent with previous finding in grass carp ( Cai et al, 2020 ).…”

Section: Discussionsupporting

confidence: 92%

Comparative genome-wide methylation analysis reveals epigenetic regulation of muscle development in grass carp (Ctenopharyngodon idellus) fed with whole faba bean

Li¹,

Fu²,

Zhang³

et al. 2022

PeerJ

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Crisp grass carp (CGC), the most representative improved varieties of grass carp (GC), features higher muscle hardness after feeding faba bean (Vicia faba L.) for 90–120 days. DNA methylation, a most widely studied epigenetic modification, plays an essential role in muscle development. Previous studies have identified numerous differentially expressed genes (DEGs) between CGC and GC. However, it remains unknown if the expression levels of these DEGs are influenced by DNA methylation. In the present study, we performed a comprehensive analysis of DNA methylation profiles between CGC and GC, and identified important candidate genes related to muscle development coupled with the transcriptome sequencing data. A total of 9,318 differentially methylated genes (DMGs) corresponding to 155,760 differentially methylated regions (DMRs) were identified between the two groups under the CG context in promoter regions. Combined with the transcriptome sequencing data, 14 key genes related to muscle development were identified, eight of which (gsk3b, wnt8a, wnt11, axin2, stat1, stat2, jak2, hsp90) were involved in muscle fiber hyperplasia, six of which (tgf-β1, col1a1, col1a2, col1a3, col4a1, col18a1) were associated with collagen synthesis in crisp grass carp. The difference of methylation levels in the key genes might lead to the expression difference, further resulting in the increase of muscle hardness in crisp grass carp. Overall, this study can help further understand how faba bean modulates muscle development by the epigenetic modifications, providing novel insights into the texture quality improvement in other aquaculture fish species by nutritional programming.

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“…Nucleotide methylation carries essential information for gene regulation, especially DNA 5-cytosine methylation (5mC) and RNA N6-adenosine methylation (m 6 A). Several previous studies indicated the essential roles of 5mC [ 23 , 35 ] and m 6 A regulation [ 35 , 36 ] during skeletal muscle development and growth, respectively. Our previous in-house study has revealed an overall decrease in DNA methylation level from the embryo to the adult pig skeletal muscle, which was highly correlated with the downregulated expression of DNMT1 [ 23 ].…”

Section: Discussionmentioning

confidence: 99%

Coordinated transcriptional and post-transcriptional epigenetic regulation during skeletal muscle development and growth in pigs

Zhang

et al. 2022

J Animal Sci Biotechnol

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Background N6-methyladenosine (m6A) and DNA 5-methylcytosine (5mC) methylation plays crucial roles in diverse biological processes, including skeletal muscle development and growth. Recent studies unveiled a potential link between these two systems, implicating the potential mechanism of coordinated transcriptional and post-transcriptional regulation in porcine prenatal myogenesis and postnatal skeletal muscle growth. Methods Immunofluorescence and co-IP assays were carried out between the 5mC writers and m6A writers to investigate the molecular basis underneath. Large-scale in-house transcriptomic data were compiled for applying weighted correlation network analysis (WGCNA) to identify the co-expression patterns of m6A and 5mC regulators and their potential role in pig myogenesis. Whole-genome bisulfite sequencing (WGBS) and methylated RNA immunoprecipitation sequencing (MeRIP-seq) were performed on the skeletal muscle samples from Landrace pigs at four postnatal growth stages (days 30, 60, 120 and 180). Results Significantly correlated expression between 5mC writers and m6A writers and co-occurrence of 5mC and m6A modification were revealed from public datasets of C2C12 myoblasts. The protein-protein interactions between the DNA methylase and the m6A methylase were observed in mouse myoblast cells. Further, by analyzing transcriptome data comprising 81 pig skeletal muscle samples across 27 developmental stages, we identified a 5mC/m6A epigenetic module eigengene and decoded its potential functions in pre- or post-transcriptional regulation in postnatal skeletal muscle development and growth of pigs. Following integrative multi-omics analyses on the WGBS methylome data and MeRIP-seq data for both m6A and gene expression profiles revealed a genome/transcriptome-wide correlated dynamics and co-occurrence of 5mC and m6A modifications as a consequence of 5mC/m6A crosstalk in the postnatal myogenesis progress of pigs. Last, we identified a group of myogenesis-related genes collaboratively regulated by both 5mC and m6A modifications in postnatal skeletal muscle growth in pigs. Conclusions Our study discloses a potential epigenetic mechanism in skeletal muscle development and provides a novel direction for animal breeding and drug development of related human muscle-related diseases.

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Genome-wide DNA methylation profiles provide insight into epigenetic regulation of red and white muscle development in Chinese perch Siniperca chuatsi

Cited by 19 publications

References 54 publications

Fertilization by short-term stored sperm alters DNA methylation patterns in common carp (Cyprinus carpio) embryos at single-base resolution

Fertilization by short-term stored sperm alters DNA methylation patterns in common carp (Cyprinus carpio) embryos at single-base resolution

Comparative genome-wide methylation analysis reveals epigenetic regulation of muscle development in grass carp (Ctenopharyngodon idellus) fed with whole faba bean

Coordinated transcriptional and post-transcriptional epigenetic regulation during skeletal muscle development and growth in pigs

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