The epigenetic trans-silencing effect in Drosophila involves maternally-transmitted small RNAs whose production depends on the piRNA pathway and HP1

• Published in: PloS one 2010-06, Vol.5 (6), p.e11032-e11032
• Main Authors: Todeschini, Anne-Laure, Teysset, Laure, Delmarre, Valérie, Ronsseray, Stéphane
• Format: Article
• Language: English
• Subjects: Analysis; Animals; Defects; Deoxyribonucleic acid; Disease transmission; DNA; DNA methylation; Drosophila; Drosophila - genetics; Drosophila melanogaster; E coli; Epigenesis, Genetic; Epigenetic inheritance; Epigenetics; Euchromatin; Female; Gene Silencing; Genes; Genetic analysis; Genetic research; Genetics; Genetics and Genomics/Chromosome Biology; Genetics and Genomics/Epigenetics; Genetics and Genomics/Gene Expression; Genomic Imprinting; Heterochromatin; Heterochromatin - genetics; Homology; Insects; Life Sciences; Meiosis; Mutation; Ovaries; Ovary - metabolism; P elements; Phenotype; Ribonucleic acid; RNA; RNA - genetics; RNA-mediated interference; Schizosaccharomyces pombe; Transgenes; Transposons; Variegation
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0011032

The study of P transposable element repression in Drosophila melanogaster led to the discovery of the Trans-Silencing Effect (TSE), a homology-dependent repression mechanism by which a P-transgene inserted in subtelomeric heterochromatin (Telomeric Associated Sequences, "TAS") has the capacity to repress in trans, in the female germline, a homologous P-lacZ transgene located in euchromatin. Phenotypic and genetic analysis have shown that TSE exhibits variegation in ovaries, displays a maternal effect as well as epigenetic transmission through meiosis and involves heterochromatin (including HP1) and RNA silencing. Here, we show that mutations in squash and zucchini, which are involved in the piwi-interacting RNA (piRNA) silencing pathway, strongly affect TSE. In addition, we carried out a molecular analysis of TSE and show that silencing is correlated to the accumulation of lacZ small RNAs in ovaries. Finally, we show that the production of these small RNAs is sensitive to mutations affecting squash and zucchini, as well as to the dose of HP1. Thus, our results indicate that the TSE represents a bona fide piRNA-based repression. In addition, the sensitivity of TSE to HP1 dose suggests that in Drosophila, as previously shown in Schizosaccharomyces pombe, a RNA silencing pathway can depend on heterochromatin components.