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Stable Polycomb-dependent transgenerational inheritance of chromatin states in Drosophila

ABSTRACT: Transgenerational epigenetic inheritance entails transmission of epigenetically determined phenotypic traits through multiple generations. However, very little is known on the principles and the mechanisms governing this type of inheritance. Here, we established stable and isogenic Drosophila epilines by transiently enhancing long-range chromatin interactions. Such epilines display two opposing chromatin states, which depend on differential levels of the H3K27me3 histone mark. Once established, both the active and the repressed epialleles can dominantly be transmitted to naïve flies and can induce paramutation. Importantly, both epilines can be reset to an intermediate naïve state by disrupting chromatin interactions. Finally, we show that the environment can modulate the expressivity of the epialleles and we extend our paradigm to naturally occurring genetic makeups. Our work sheds light on how nuclear organization contributes to epigenetically heritable phenotypic variability and therefore to evolution.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE76799 | GEO | 2017/03/14

SECONDARY ACCESSION(S): PRJNA308609

REPOSITORIES: GEO

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Project description:Phenotypic differences caused by epimutations rather than changes in DNA sequence have been described in various organisms. Epimutations are potentially adaptive if inherited across generations and might even respond to environmental challenges. Yet experimental evidence is scarce1. Examples of heritable phenotypic changes are paramutation in plants and RNA-induced epigenetic silencing (RNAe) in nematodes, in which small RNAs trigger the formation of silent epialleles that are stable across generations2-7. Consequently, RNA-directed epimutagenesis has been associated with persistent gene repression. Here, using the fission yeast Schizosaccharomyces pombe, we demonstrate that RNA-induced epimutations are stably transmitted to subsequent generations also after reactivation of the silenced gene. This enables descendants to remember and reinstate preceding silencing episodes that had occurred in their ancestors. We show that temporary expression of hairpin-derived small interfering RNAs (siRNAs) triggers RNAe that is stably propagated for at least 18 generations upon inactivation of the polymerase-associated factor 1 complex (Paf1C). In the presence of Paf1C, the silent state is lost, but resumes if Paf1C is again impaired, even in the absence of the original trigger and in later generations. Thus, in yeast RNAe installs a molecular imprint that can be inherited through meiosis with no discernible phenotypic consequences. We show that trimethylated histone H3 lysine 9 (H3K9me3) is a major constituent of this imprint, and that stable propagation thereof is coupled to RNA interference (RNAi). Our findings reveal a distinct form of epigenetic memory in which fission yeast cells acquire heritable, transcriptionally active epialleles that confer gene silencing and manifest a phenotype only in particular, recurring situations. This demonstrates that epigenetic inheritance is adaptive and could potentially constitute a strategy to cope with adverse environmental conditions. If conserved in other eukaryotes, this phenomenon will impact our comprehension of natural variation and epigenetics in evolution.

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Stable Polycomb-dependent transgenerational inheritance of chromatin states in Drosophila

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