A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex

Kvist, Jouni; Athanàsio, Camila Gonçalves; Pfrender, Michael E.; Brown, James B.; Colbourne, John K.; Mirbahai, Leda

doi:10.1186/s12864-019-6415-5

Title: A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex

Journal Article · Mon Jan 06 00:00:00 EST 2020 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-019-6415-5· OSTI ID:1626826

Kvist, Jouni ^[1]; Athanàsio, Camila Gonçalves ^[2]; Pfrender, Michael E. ^[3]; Brown, James B. ^[4]; Colbourne, John K. ^[5]; Mirbahai, Leda ^[6]

Univ. of Helsinki (Finland). Research Program for Molecular Neurology
McGill Univ., Montreal, QC (Canada). Dept. of Natural Resource Sciences
Univ. of Notre Dame, IN (United States). Dept. of Biological Sciences and Environmental Change Initiative
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology; Univ. of Birmingham (United Kingdom). Centre for Computational Biology (CCB)
Univ. of Birmingham (United Kingdom). School of Biosciences
Univ. of Warwick, Coventry (United Kingdom). Warwick Medical School

BACKGROUND:Daphnia species reproduce by cyclic parthenogenesis involving both sexual and asexual reproduction. The sex of the offspring is environmentally determined and mediated via endocrine signalling by the mother. Interestingly, male and female Daphnia can be genetically identical, yet display large differences in behaviour, morphology, lifespan and metabolic activity. Our goal was to integrate multiple omics datasets, including gene expression, splicing, histone modification and DNA methylation data generated from genetically identical female and male Daphnia pulex under controlled laboratory settings with the aim of achieving a better understanding of the underlying epigenetic factors that may contribute to the phenotypic differences observed between the two genders. RESULTS:In this study we demonstrate that gene expression level is positively correlated with increased DNA methylation, and histone H3 trimethylation at lysine 4 (H3K4me3) at predicted promoter regions. Conversely, elevated histone H3 trimethylation at lysine 27 (H3K27me3), distributed across the entire transcript length, is negatively correlated with gene expression level. Interestingly, male Daphnia are dominated with epigenetic modifications that globally promote elevated gene expression, while female Daphnia are dominated with epigenetic modifications that reduce gene expression globally. For examples, CpG methylation (positively correlated with gene expression level) is significantly higher in almost all differentially methylated sites in male compared to female Daphnia. Furthermore, H3K4me3 modifications are higher in male compared to female Daphnia in more than 3/4 of the differentially regulated promoters. On the other hand, H3K27me3 is higher in female compared to male Daphnia in more than 5/6 of differentially modified sites. However, both sexes demonstrate roughly equal number of genes that are up-regulated in one gender compared to the other sex. Since, gene expression analyses typically assume that most genes are expressed at equal level among samples and different conditions, and thus cannot detect global changes affecting most genes. CONCLUSIONS:The epigenetic differences between male and female in Daphnia pulex are vast and dominated by changes that promote elevated gene expression in male Daphnia. Furthermore, the differences observed in both gene expression changes and epigenetic modifications between the genders relate to pathways that are physiologically relevant to the observed phenotypic differences.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Wellcome Trust

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626826

Alternate ID(s):: OSTI ID: 1765554

Journal Information:: BMC Genomics, Vol. 21, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 17 works

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A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.c.4806849 The current record is supplemented by this collection	collection	January 2020
MOESM2 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531142.v1 The current record is supplemented by this dataset	dataset	January 2020
MOESM1 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531130 The current record is supplemented by this dataset	dataset	January 2020
A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.c.4806849.v1 The current record is supplemented by this collection	collection	January 2020
MOESM1 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531130.v1 The current record is supplemented by this dataset	dataset	January 2020
MOESM3 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531148 The current record is supplemented by this text	text	January 2020
MOESM2 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531142 The current record is supplemented by this dataset	dataset	January 2020
MOESM3 of A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex Kvist, Jouni; Athanàsio, Camila; Pfrender, Michael https://doi.org/10.6084/m9.figshare.11531148.v1 The current record is supplemented by this text	text	January 2020

Title: A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex

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