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Epigenetics Volume 18, 2023 - Issue 1
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Research Paper

Coordinated alternation of DNA methylation and alternative splicing of PBRM1 affect bovine sperm structure and motility

Chunhong Yanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Yao Xiaoa Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Xiuge Wanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Xiaochao Weia Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Jinpeng Wanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Yaping Gaoa Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Qiang Jianga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Zhihua Jua Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.China;c College of Life Sciences, Shandong Normal University, Jinan, P. R. ChinaView further author information
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Yaran Zhanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Wenhao Liua Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Ning Huanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Yanqin Lia Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Yundong Gaoa Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Lingling Wanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.ChinaView further author information
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Jinming Huanga Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan, P. R. China;b Shandong Key Laboratory of Animal Disease Control and Breeding, Jinan, P.R.China;c College of Life Sciences, Shandong Normal University, Jinan, P. R. ChinaCorrespondence[email protected]
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Article: 2183339 | Received 23 Aug 2022, Accepted 15 Feb 2023, Published online: 03 Mar 2023
 
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ABSTRACT

DNA methylation and gene alternative splicing drive spermatogenesis. In screening DNA methylation markers and transcripts related to sperm motility, semen from three pairs of full-sibling Holstein bulls with high and low motility was subjected to reduced representation bisulphite sequencing. A total of 948 DMRs were found in 874 genes (gDMRs). Approximately 89% of gDMR-related genes harboured alternative splicing events, including SMAD2, KIF17, and PBRM1. One DMR in exon 29 of PBRM1 with the highest 5mC ratio was found, and hypermethylation in this region was related to bull sperm motility. Furthermore, alternative splicing events at exon 29 of PBRM1 were found in bull testis, including PBRM1-complete, PBRM1-SV1 (exon 28 deletion), and PBRM1-SV2 (exons 28–29 deletion). PBRM1-SV2 exhibited significantly higher expression in adult bull testes than in newborn bull testes. In addition, PBRM1 was localized to the redundant nuclear membrane of bull sperm, which might be related to sperm motility caused by sperm tail breakage. Therefore, the hypermethylation of exon 29 may be associated with the production of PBRM1-SV2 in spermatogenesis. These findings indicated that DNA methylation alteration at specific loci could regulate gene splicing and expression and synergistically alter sperm structure and motility.

Disclosure statement

No potential conflict of interest was reported by the author(s)

Ethical approval statement:

All protocols for collecting samples from bulls were reviewed and approved by the Animal Care and Use Committee of Shandong Academy of Agricultural Sciences. The experiment was conducted under the regulations and guidelines established by this committee.

Availability of data and materials

The raw data of RRBS has been uploaded to the NCBI SRA, and the accession number was PRJNA818321.

Author contributions

J.H. conceived and designed the experiments. C.Y., X.Y., X.W., X.C.W., J.W., Z.J., and N.H. performed experiments and analyzed data. Q.J., Y.Z., W.L., L.W., Y.L., and Y.G. collected bull samples and prepared materials. C.Y. and J.H. wrote the manuscript. All the authors read and approved the final manuscript.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15592294.2023.2183339

Additional information

Funding

This work was supported by the National Key Research and Development Program of China (grant number 2021YFF1000703), National Natural Science Foundation of China (grant number 32002182), Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2022A05), Shandong Key Research and Development Program (2021LZGC011); and Shandong Agricultural Elite Variety Project (grant number 2019LZGC011).
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