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Genetics. 2016 Oct;204(2):631-644. Epub 2016 Aug 24.

Production of Small Noncoding RNAs from the flamenco Locus Is Regulated by the gypsy Retrotransposon of Drosophila melanogaster.

Author information

1
Institute of Biosciences and Bioresources, Consiglio Nazionale delle Ricerche, 80131 Naples, Italy.
2
Division of Molecular Biology, Biomedical Center and Center for Integrated Protein Science Munich, Ludwig-Maximilians-University, 82152 Planegg-Martinsried, Germany.
3
Institute of Genetics and Biophysics "Adriano Buzzati Traverso," Consiglio Nazionale delle Ricerche, 80131 Naples, Italy.
4
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 113-0032, Japan.
5
Institute of Biosciences and Bioresources, Consiglio Nazionale delle Ricerche, 80131 Naples, Italy Institute of Molecular Genetics, Consiglio Nazionale delle Ricerche, 40136 Bologna, Italy SC Laboratory of Musculoskeletal Cell Biology, Rizzoli Orthopedic Institute, 40136 Bologna, Italy dandrena@area.bo.cnr.it.

Abstract

Protective mechanisms based on RNA silencing directed against the propagation of transposable elements are highly conserved in eukaryotes. The control of transposable elements is mediated by small noncoding RNAs, which derive from transposon-rich heterochromatic regions that function as small RNA-generating loci. These clusters are transcribed and the precursor transcripts are processed to generate Piwi-interacting RNAs (piRNAs) and endogenous small interfering RNAs (endo-siRNAs), which silence transposable elements in gonads and somatic tissues. The flamenco locus is a Drosophila melanogaster small RNA cluster that controls gypsy and other transposable elements, and has played an important role in understanding how small noncoding RNAs repress transposable elements. In this study, we describe a cosuppression mechanism triggered by new euchromatic gypsy insertions in genetic backgrounds carrying flamenco alleles defective in gypsy suppression. We found that the silencing of gypsy is accompanied by the silencing of other transposons regulated by flamenco, and of specific flamenco sequences from which small RNAs against gypsy originate. This cosuppression mechanism seems to depend on a post-transcriptional regulation that involves both endo-siRNA and piRNA pathways and is associated with the occurrence of developmental defects. In conclusion, we propose that new gypsy euchromatic insertions trigger a post-transcriptional silencing of gypsy sense and antisense sequences, which modifies the flamenco activity. This cosuppression mechanism interferes with some developmental processes, presumably by influencing the expression of specific genes.

KEYWORDS:

RNA silencing; ecdysis; primary transcript; small RNA; transposon

PMID:
27558137
PMCID:
PMC5068851
DOI:
10.1534/genetics.116.187922
[Indexed for MEDLINE]
Free PMC Article

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