Heterochromatin protein 1a functions for piRNA biogenesis predominantly from pericentric and telomeric regions in Drosophila

Ryan Yee Wei Teo,Katsutomo Okamura,Amit Anand,Vishweshwaren Sridhar,Toshie Kai

doi:10.1038/s41467-018-03908-3

Abstract

In metazoan germline, Piwi-interacting RNAs (piRNAs) provide defence against transposons. Piwi–piRNA complex mediates transcriptional silencing of transposons in nucleus. Heterochromatin protein 1a (HP1a) has been proposed to function downstream of Piwi-piRNA complex in Drosophila. Here we show that HP1a germline knockdown (HP1a-GLKD) leads to a reduction in the total and Piwi-bound piRNAs mapping to clusters and transposons insertions, predominantly in the regions close to telomeres and centromeres, resulting in derepression of a limited number of transposons from these regions. In addition, HP1a-GLKD increases the splicing of transcripts arising from clusters in above regions, suggesting HP1a also functions upstream to piRNA processing. Evolutionarily old transposons enriched in the pericentric regions exhibit significant loss in piRNAs targeting these transposons upon HP1a-GLKD. Our study suggests that HP1a functions to repress transposons in a chromosomal compartmentalised manner.

Highlights

In metazoan germline, Piwi-interacting RNAs provide defence against transposons
Heterochromatin protein 1a (HP1a) was shown to repress transposon expression and is believed to exert its functions downstream of Piwi-piRISC, its function in the Piwi-interacting RNAs (piRNAs) pathway in germline has not been investigated in detail13
We cannot exclude a possibility of milder effect due to incomplete knockdown, we show that HP1a functions in piRNA biogenesis and upstream to piRNA-mediated transcriptional repression

Summary

Introduction

Piwi-interacting RNAs (piRNAs) provide defence against transposons. Heterochromatin protein 1a (HP1a) has been proposed to function downstream of Piwi-piRNA complex in Drosophila. A nuclear protein, Panoramix (Panx) mediates PiwipiRISC-directed recruitment of dSETDB1/Egg, a histone methyltransferase, at the transposon loci for H3K9 trimethylation14,15 Another reported Piwi partner, the conserved heterochromatin protein, Heterochromatin Protein 1a (HP1a) has been proposed as a downstream factor to enforce transposon silencing in the Drosophila germline and ovarian somatic cells. HP1a binding was shown to lead to the repression of transposon loci, which is most likely based on its ability to recruit the Egg protein14,17–19 This suggests that HP1a may play its roles downstream of the piRNA pathway. We examined the function of HP1a in the piRNA pathway and transposon repression in the Drosophila female germline cells. We show that HP1a functions upstream to piRNA processing, likely by repressing splicing of piRNA precursors

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Conclusion