Comparative whole genome DNA methylation profiling of cattle sperm and somatic tissues reveals striking hypomethylated patterns in sperm

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Abstract

Background

Although sperm DNA methylation has been studied in humans and other species, its status in cattle is largely unknown.

Results

Using whole-genome bisulfite sequencing (WGBS), we profiled the DNA methylome of cattle sperm through comparison with three somatic tissues (mammary gland, brain, and blood). Large differences between cattle sperm and somatic cells were observed in the methylation patterns of global CpGs, pericentromeric satellites, partially methylated domains (PMDs), hypomethylated regions (HMRs), and common repeats. As expected, we observed low methylation in the promoter regions and high methylation in the bodies of active genes. We detected selective hypomethylation of megabase domains of centromeric satellite clusters, which may be related to chromosome segregation during meiosis and their rapid transcriptional activation upon fertilization. We found more PMDs in sperm cells than in somatic cells and identified meiosis-related genes such as KIF2B and REPIN1, which are hypomethylated in sperm but hypermethylated in somatic cells. In addition to the common HMRs around gene promoters, which showed substantial differences between sperm and somatic cells, the sperm-specific HMRs also targeted to distinct spermatogenesis-related genes, including BOLL, MAEL, ASZ1, SYCP3, CTCFL, MND1, SPATA22, PLD6, DDX4, RBBP8, FKBP6, and SYCE1. Although common repeats were heavily methylated in both sperm and somatic cells, some young Bov-A2 repeats, which belong to the SINE family, were hypomethylated in sperm and could affect the promoter structures by introducing new regulatory elements.

Conclusions

Our study provides a comprehensive resource for bovine sperm epigenomic research and enables new discoveries about DNA methylation and its role in male fertility.

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Most cited references 57

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Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

Shawn Cokus, Suhua Feng, Xiaoyu Zhang … (2008)

Cytosine DNA methylation is important in regulating gene expression and in silencing transposons and other repetitive sequences. Recent genomic studies in Arabidopsis thaliana have revealed that many endogenous genes are methylated either within their promoters or within their transcribed regions, and that gene methylation is highly correlated with transcription levels. However, plants have different types of methylation controlled by different genetic pathways, and detailed information on the methylation status of each cytosine in any given genome is lacking. To this end, we generated a map at single-base-pair resolution of methylated cytosines for Arabidopsis, by combining bisulphite treatment of genomic DNA with ultra-high-throughput sequencing using the Illumina 1G Genome Analyser and Solexa sequencing technology. This approach, termed BS-Seq, unlike previous microarray-based methods, allows one to sensitively measure cytosine methylation on a genome-wide scale within specific sequence contexts. Here we describe methylation on previously inaccessible components of the genome and analyse the DNA methylation sequence composition and distribution. We also describe the effect of various DNA methylation mutants on genome-wide methylation patterns, and demonstrate that our newly developed library construction and computational methods can be applied to large genomes such as that of mouse.

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Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L.

Déborah Bourc'his, Timothy Bestor (2004)

Mammalian genomes employ heritable cytosine methylation in the long-term silencing of retrotransposons and genes subject to genomic imprinting and X chromosome inactivation. Little is known of the mechanisms that direct cytosine methylation to specific sequences. Here we show that DNA methyltransferase 3-like (Dnmt3L (ref. 1)) is expressed in testes during a brief perinatal period in the non-dividing precursors of spermatogonial stem cells at a stage where retrotransposons undergo de novo methylation. Deletion of the Dnmt3L gene prevented the de novo methylation of both long-terminal-repeat (LTR) and non-LTR retrotransposons, which were transcribed at high levels in spermatogonia and spermatocytes. Loss of Dnmt3L from early germ cells also caused meiotic failure in spermatocytes, which do not express Dnmt3L. Whereas dispersed repeated sequences were demethylated in mutant germ cells, tandem repeats in pericentric regions were methylated normally. This result indicates that the Dnmt3L protein might have a function in the de novo methylation of dispersed repeated sequences in a premeiotic genome scanning process that occurs in male germ cells at about the time of birth.

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Epigenetic reprogramming in mouse primordial germ cells.

Petra Hajkova, Sylvia Erhardt, Natasha E. Lane … (2002)

Genome-wide epigenetic reprogramming in mammalian germ cells, zygote and early embryos, plays a crucial role in regulating genome functions at critical stages of development. We show here that mouse primordial germ cells (PGCs) exhibit dynamic changes in epigenetic modifications between days 10.5 and 12.5 post coitum (dpc). First, contrary to previous suggestions, we show that PGCs do indeed acquire genome-wide de novo methylation during early development and migration into the genital ridge. However, following their entry into the genital ridge, there is rapid erasure of DNA methylation of regions within imprinted and non-imprinted loci. For most genes, the erasure commences simultaneously in PGCs in both male and female embryos, which is completed within 1 day of development. Based on the kinetics of this process, we suggest that this is an active demethylation process initiated upon the entry of PGCs into the gonadal anlagen. The timing of reprogramming in PGCs is crucial since it ensures that germ cells of both sexes acquire an equivalent epigenetic state prior to the differentiation of the definitive male and female germ cells in which new parental imprints are established subsequently. Some repetitive elements, however, show incomplete erasure, which may be essential for chromosome stability and for preventing activation of transposons to reduce the risk of germline mutations. Aberrant epigenetic reprogramming in the germ line would cause the inheritance of epimutations that may have consequences for human diseases as suggested by studies on mouse models. Copyright 2002 Elsevier Science Ireland Ltd.

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Author and article information

Journal

Journal ID (nlm-ta): Gigascience

Journal ID (iso-abbrev): Gigascience

Journal ID (publisher-id): gigascience

Title: GigaScience

Publisher: Oxford University Press

ISSN (Electronic): 2047-217X

Publication date (Electronic): 10 April 2018

Publication date Collection: May 2018

Publication date PMC-release: 10 April 2018

Volume: 7

Issue: 5

Electronic Location Identifier: giy039

Affiliations

[1 ]Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, Huazhong Agricultural University, Wuhan, Hubei, 430070, China

[2 ]Animal Genomics and Improvement Laboratory, BARC, US Department of Agriculture, Agriculture Research Service, Beltsville, MD 20705, USA

[3 ]The Cell Wall Utilization and Biology Laboratory, US Department of Agriculture, Agriculture Research Service, Madison, WI, 53706, USA

Author notes

Correspondence address. Animal Genomics and Improvement Laboratory, US Department of Agriculture, Agriculture Research Service, Building 306, Room 111, BARC-East, Beltsville, MD 20705, USA. Tel: +1-301-504-9843; Fax: +1-301-504-8414; E-mail: George.Liu@ 123456ars.usda.gov

Author information

George E Liu http://orcid.org/0000-0003-0192-6705

Article

Publisher ID: giy039

DOI: 10.1093/gigascience/giy039

PMC ID: 5928411

PubMed ID: 29635292

SO-VID: 945a090d-7417-4438-b242-175caf2b55eb

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date accepted : 28 March 2018

Date received : 07 November 2017

Date revision received : 02 February 2018

Page count

Pages: 13

Funding

Funded by: Agriculture and Food Research Initiative (AFRI)

Award ID: 2013-67015-20951

Funded by: Binational Agricultural Research and Development (BARD) 10.13039/100006031

Comparative whole genome DNA methylation profiling of cattle sperm and somatic tissues reveals striking hypomethylated patterns in sperm

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Abstract

Background

Results

Conclusions

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Genome Integrity

Most cited references 57

Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L.

Epigenetic reprogramming in mouse primordial germ cells.

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