Abstract
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.
Highlights
The idea that gene–environment interactions (GxE), not the genotype (G) alone, underpin the expression of the phenotype is well established [1,2,3]
Cytoplasms Differ in Mitochondrial Genomes and Wolbachia Presence
While the result is replicated across two replicate lines and so is relatively robust against individual variation, we note that our data do not allow any conclusions as to which tissues are responsible of the observed overall epigenetic changes
Summary
The idea that gene–environment interactions (GxE), not the genotype (G) alone, underpin the expression of the phenotype is well established [1,2,3] Based on this GxE→P idea, we and others developed a more general concept based on systems biology stating that G is an inheritance system that includes other interacting and heritable components including the epigenome and cytoplasmic components such as mitochondria, Wolbachia, and viruses [4,5,6,7]. Sequence differences in the genomes of cytoplasmic elements such as mitochondria, which interact with the nucleus, may drive variation in the nuclear genome and the epigenome Considering these heritable interaction effects on the phenotype is important because they can be as strong as the effects by the individual cytoplasmic components [8]
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