Certain RNAs are transmitted from one generation to the next and can provide an ideal means to transmit epigenetic memory. Indeed, in Drosophila piRNA-Piwi complexes are deposited into the oocytes and are present in the early embryo. These piRNA-Piwi complexes accumulate in the pole plasm, which gives rise to the gonads. Inherited piRNAs carry epigenetic information that determines target silencing in the progeny, but the mechanism by which the piRNAs impact targets was not known. In close collaboration, the Aravin lab and we have shown that inherited piRNAs affect the chromatin of target loci. We used D. melanogaster strains, which contain an identical transgene inserted into two different genomic loci. Germ cells generate abundant piRNAs from the transgene in one locus, while not from the other locus. Importantly, the inactive locus can be converted into an “active” locus by exposure to maternally inherited cytoplasm, carrying piRNAs homologous to the locus (deposited by the mother carrying the active locus).   We found that the production of piRNAs from the active locus and conversion of the inactive locus to an active one (mediated by trans-generational piRNAs), was accompanied by an increase in H3K9me3 on the transgene. Therefore, exposure of an inactive locus to homologous piRNAs inherited from the previous generation leads to installment of H3K9me3 and conversion of the locus to an active piRNA-producing locus.  

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