A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex
Abstract
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 sitesmore »
- Authors:
-
- 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
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Wellcome Trust
- OSTI Identifier:
- 1626826
- Alternate Identifier(s):
- OSTI ID: 1765554
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- BMC Genomics
- Additional Journal Information:
- Journal Volume: 21; Journal Issue: 1; Journal ID: ISSN 1471-2164
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biotechnology & applied microbiology; genetics & heredity; epigenetics; gene expression; evolution; non-conventional model organisms
Citation Formats
Kvist, Jouni, Athanàsio, Camila Gonçalves, Pfrender, Michael E., Brown, James B., Colbourne, John K., and Mirbahai, Leda. A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex. United States: N. p., 2020.
Web. doi:10.1186/s12864-019-6415-5.
Kvist, Jouni, Athanàsio, Camila Gonçalves, Pfrender, Michael E., Brown, James B., Colbourne, John K., & Mirbahai, Leda. A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex. United States. https://doi.org/10.1186/s12864-019-6415-5
Kvist, Jouni, Athanàsio, Camila Gonçalves, Pfrender, Michael E., Brown, James B., Colbourne, John K., and Mirbahai, Leda. Mon .
"A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex". United States. https://doi.org/10.1186/s12864-019-6415-5. https://www.osti.gov/servlets/purl/1626826.
@article{osti_1626826,
title = {A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex},
author = {Kvist, Jouni and Athanàsio, Camila Gonçalves and Pfrender, Michael E. and Brown, James B. and Colbourne, John K. and Mirbahai, Leda},
abstractNote = {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.},
doi = {10.1186/s12864-019-6415-5},
journal = {BMC Genomics},
number = 1,
volume = 21,
place = {United States},
year = {Mon Jan 06 00:00:00 EST 2020},
month = {Mon Jan 06 00:00:00 EST 2020}
}
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EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments
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Gene Body Methylation Patterns in Daphnia Are Associated with Gene Family Size
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Epigenetic Potential as a Mechanism of Phenotypic Plasticity in Vertebrate Range Expansions
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