The Cytoplasm Affects the Epigenome in Drosophila melanogaster

Cytoplasmic components and their interactions with the nuclear genome may mediate patterns of phenotypic expression to form a joint inheritance system. However, proximate mechanisms underpinning these interactions remain elusive. To independently assess nuclear genetic and epigenetic cytoplasmic eff...

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Main Authors: Christoph Grunau, Susanne Voigt, Ralph Dobler, Damian K. Dowling, Klaus Reinhardt
Format: Article
Language:English
Published: MDPI AG 2018-09-01
Series:Epigenomes
Subjects:
Online Access:http://www.mdpi.com/2075-4655/2/3/17
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spelling doaj-6ba63ae93d5c40a69d79c0e591204ce92021-04-02T11:03:37ZengMDPI AGEpigenomes2075-46552018-09-01231710.3390/epigenomes2030017epigenomes2030017The Cytoplasm Affects the Epigenome in Drosophila melanogasterChristoph Grunau0Susanne Voigt1Ralph Dobler2Damian K. Dowling3Klaus Reinhardt4IHPE UMR 5244, University Perpignan Via Domitia, CNRS, IFREMER, University Montpellier, F-66860 Perpignan, FranceApplied Zoology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, GermanyApplied Zoology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, GermanySchool of Biological Sciences, Monash University, Clayton, VIC 3800, AustraliaApplied Zoology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, GermanyCytoplasmic components and their interactions with the nuclear genome may mediate patterns of phenotypic expression to form a joint inheritance system. However, proximate mechanisms underpinning these interactions remain elusive. To independently assess nuclear genetic and epigenetic cytoplasmic effects, we created a full-factorial design in which representative cytoplasms and nuclear backgrounds from each of two geographically disjunct populations of Drosophila melanogaster were matched together in all four possible combinations. To capture slowly-accumulating epimutations in addition to immediately occurring ones, these constructed populations were examined one year later. We found the K4 methylation of histone H3, H3K4me3, an epigenetic marker associated with transcription start-sites had diverged across different cytoplasms. The loci concerned mainly related to metabolism, mitochondrial function, and reproduction. We found little overlap (<8%) in sites that varied genetically and epigenetically, suggesting that epigenetic changes have diverged independently from any cis-regulatory sequence changes. These results are the first to show cytoplasm-specific effects on patterns of nuclear histone methylation. Our results highlight that experimental nuclear-cytoplasm mismatch may be used to provide a platform to identify epigenetic candidate loci to study the molecular mechanisms of cyto-nuclear interactions.http://www.mdpi.com/2075-4655/2/3/17epigeneticsmitochondriamito-nuclear coevolutionWolbachia
collection DOAJ
language English
format Article
sources DOAJ
author Christoph Grunau
Susanne Voigt
Ralph Dobler
Damian K. Dowling
Klaus Reinhardt
spellingShingle Christoph Grunau
Susanne Voigt
Ralph Dobler
Damian K. Dowling
Klaus Reinhardt
The Cytoplasm Affects the Epigenome in Drosophila melanogaster
Epigenomes
epigenetics
mitochondria
mito-nuclear coevolution
Wolbachia
author_facet Christoph Grunau
Susanne Voigt
Ralph Dobler
Damian K. Dowling
Klaus Reinhardt
author_sort Christoph Grunau
title The Cytoplasm Affects the Epigenome in Drosophila melanogaster
title_short The Cytoplasm Affects the Epigenome in Drosophila melanogaster
title_full The Cytoplasm Affects the Epigenome in Drosophila melanogaster
title_fullStr The Cytoplasm Affects the Epigenome in Drosophila melanogaster
title_full_unstemmed The Cytoplasm Affects the Epigenome in Drosophila melanogaster
title_sort cytoplasm affects the epigenome in drosophila melanogaster
publisher MDPI AG
series Epigenomes
issn 2075-4655
publishDate 2018-09-01
description Cytoplasmic components and their interactions with the nuclear genome may mediate patterns of phenotypic expression to form a joint inheritance system. However, proximate mechanisms underpinning these interactions remain elusive. To independently assess nuclear genetic and epigenetic cytoplasmic effects, we created a full-factorial design in which representative cytoplasms and nuclear backgrounds from each of two geographically disjunct populations of Drosophila melanogaster were matched together in all four possible combinations. To capture slowly-accumulating epimutations in addition to immediately occurring ones, these constructed populations were examined one year later. We found the K4 methylation of histone H3, H3K4me3, an epigenetic marker associated with transcription start-sites had diverged across different cytoplasms. The loci concerned mainly related to metabolism, mitochondrial function, and reproduction. We found little overlap (<8%) in sites that varied genetically and epigenetically, suggesting that epigenetic changes have diverged independently from any cis-regulatory sequence changes. These results are the first to show cytoplasm-specific effects on patterns of nuclear histone methylation. Our results highlight that experimental nuclear-cytoplasm mismatch may be used to provide a platform to identify epigenetic candidate loci to study the molecular mechanisms of cyto-nuclear interactions.
topic epigenetics
mitochondria
mito-nuclear coevolution
Wolbachia
url http://www.mdpi.com/2075-4655/2/3/17
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