PIWI-Interacting RNA in Drosophila: Biogenesis, Transposon Regulation, and Beyond

Abstract

PIWI-interacting RNAs (piRNAs) are germline-enriched small RNAs that control transposons to maintain genome integrity. To achieve this, upon being processed from piRNA precursors, most of which are transcripts of intergenic piRNA clusters, piRNAs bind PIWI proteins, germline-specific Argonaute proteins, to form effector complexes. The mechanism of this piRNA-mediated transposon silencing pathway is fundamentally similar to that of siRNA/miRNA-dependent gene silencing in that a small RNA guides its partner Argonaute protein to target gene transcripts for repression via RNA-RNA base pairing. However, the uniqueness of this piRNA pathway has emerged through intensive genetic, biochemical, bioinformatic, and structural investigations. Here, we review the studies that elucidated the piRNA pathway, mainly in Drosophila, by describing both historical and recent progress. Studies in other species that have made important contributions to the field are also described.

Regulation of Nucleolar Dominance in Drosophila melanogaster

“…However, neither piwi (P-element-induced wimpy testes) or ago3 (argonaute 3) mutants compromised nucleolar dominance in male GSCs ( Figure 3C). Piwi and Ago3 are involved in the nuclear and cytoplasmic arms of the piRNA pathway, respectively (Yamashiro and Siomi 2018). The GSCs of piwi 1 /piwi 06843 males showed no change in Y rDNA dominance (73.4 6 11.8% compared to wild-type control 70.1 6 14.9%) ( Figure 3C).…”

Requirements for multivalent Yb body assembly in transposon silencing in Drosophila

“…PIWI‐interacting RNAs (piRNAs) are engaged in an arms race with mobile transposons to maintain the genetic integrity of the germline . In Drosophila ovarian somatic cells (OSCs), transposon‐repressing piRNAs arise nearly exclusively from the uni‐strand piRNA cluster flamenco ( flam ), located at the pericentromeric region of the X chromosome .…”

Essential roles of Windei and nuclear monoubiquitination of Eggless/ SETDB 1 in transposon silencing

“…piRNAs are small non-coding RNAs enriched in the germline. piRNAs assemble the piRNA-induced silencing complexes (piRISCs) with members of the PIWI family of proteins [13][14][15][16]. piRNAs show high complementarity to transposon RNA transcripts in both sense and antisense orientations and repress transposons transcriptionally, by inducing local heterochromatinization, or post-transcriptionally, by cleaving target RNAs [13][14][15][16].…”

“…piRNAs assemble the piRNA-induced silencing complexes (piRISCs) with members of the PIWI family of proteins [13][14][15][16]. piRNAs show high complementarity to transposon RNA transcripts in both sense and antisense orientations and repress transposons transcriptionally, by inducing local heterochromatinization, or post-transcriptionally, by cleaving target RNAs [13][14][15][16]. In Drosophila ovarian somatic cells (OSCs), piRNAs assemble piRISCs solely with Piwi, the only nuclear member of the PIWI protein family, and, with multiple co-factors, transcriptionally repress transposons [12,[17][18][19][20][21].…”