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Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation

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Abstract

Enhanced pre-pubertal nutrition in Holstein bulls increased reproductive hormone production and sperm production potential with no negative effects on sperm quality. However, recent trends in human epigenetic research have identified pre-pubertal period to be critical for epigenetic reprogramming in males. Our objective was to evaluate the methylation changes in sperm of bulls exposed to different pre-pubertal diets. One-week-old Holstein bull calves (n = 9), randomly allocated to 3 groups, were fed either a high, medium or low diet (20%, 17% or 12.2% crude protein and 67.9%, 66% or 62.9% total digestible nutrients, respectively) from 2 to 32 weeks of age, followed by medium nutrition. Semen collected from bulls at two specific time points, i.e. 55–59 and 69–71 weeks, was diluted, cryopreserved and used for reduced representation bisulfite sequencing. Differential methylation was detected for dietary treatment, but minimal differences were detected with age. The gene ontology term, “regulation of Rho protein signal transduction”, implicated in sperm motility and acrosome reaction, was enriched in both low-vs-high and low-vs-medium datasets. Furthermore, several genes implicated in early embryo and foetal development showed differential methylation for diet. Our results therefore suggest that sperm epigenome keeps the memory of diet during pre-pubertal period in genes important for spermatogenesis, sperm function and early embryo development.

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Availability of data and materials

The datasets generated and/or analysed during the current study are available in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB35854 (https://www.ebi.ac.uk/ena/data/view/PRJEB35854).

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Funding

This study received funding support from the Natural Sciences and Engineering Research Council of Canada (Discovery Grant # RGPIN-2020–04585 to JT).

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Authors and Affiliations

  1. Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, T2N 4N1, Canada

    Chinju Johnson, Alysha Dance, John Kastelic & Jacob Thundathil

  2. Université Paris-Saclay, INRAE, ENVA, BREED, 78350, Jouy-en-Josas, France

    Hélène Kiefer, Aurélie Chaulot-Talmon, Luc Jouneau & Hélène Jammes

  3. R&D Department, ALLICE, 149 rue de Bercy, 75012, Paris, France

    Eli Sellem

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  1. Chinju Johnson
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  2. Hélène Kiefer
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Contributions

CJ performed the pyrosequencing experiment, participated in the RRBS experiments and data analysis and drafted the manuscript. HK and LJ performed the bioinformatics and statistical analyses of RRBS data. ACT constructed the RRBS libraries. HK, ES, AD, JK, JT and HJ participated in the conception of the study and editing of the manuscript.

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Correspondence to Chinju Johnson.

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Johnson, C., Kiefer, H., Chaulot-Talmon, A. et al. Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation. Cell Tissue Res 389, 587–601 (2022). https://doi.org/10.1007/s00441-022-03659-0

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