Genetic Interactions BetweenPElements Involved in piRNA-Mediated Repression of Hybrid Dysgenesis inDrosophila melanogaster

Abstract

Previous studies have shown that telomeric P elements inserted at the left end of the X chromosome are anchors of the P cytotype, the maternally inherited state that regulates P-element activity in the germ line of Drosophila melanogaster. This regulation is mediated by small RNAs that associate with the Piwi family of proteins (piRNAs). We extend the analysis of cytotype regulation by studying new combinations of telomeric and nontelomeric P elements (TPs and non-TPs). TPs interact with each other to enhance cytotype regulation. This synergism involves a strictly maternal effect, called presetting, which is apparently mediated by piRNAs transmitted through the egg. Presetting by a maternal TP can elicit regulation by an inactive paternally inherited TP, possibly by stimulating its production of primary piRNAs. When one TP has come from a stock heterozygous for a mutation in the aubergine, piwi, or Suppressor of variegation 205 genes, the synergism between two TPs is impaired. TPs also interact with non-TPs to enhance cytotype regulation, even though the non-TPs lack regulatory ability on their own. Non-TPs are not susceptible to presetting by a TP, nor is a TP susceptible to presetting by a non-TP. The synergism between TPs and non-TPs is stronger when the TP was inherited maternally. This synergism may be due to the accumulation of secondary piRNAs created by ping-pong cycling between primary piRNAs from the TPs and mRNAs from the non-TPs. Maternal transmission of P-element piRNAs plays an important role in the maintenance of strong cytotype regulation over generations.

Transposable elements inDrosophila

“…3A). 50,51 In addition to P elements, hobo elements and I elements (a family of non-LTR retrotransposons) play a similar role in hybrid dysgenesis when males and females of certain Drosophila strains are crossed 45 Figure 3. P element splicing and hybrid dysgenesis.…”

The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element

“…Empirical data regarding the quantitative relationship between TE copy numbers inside and outside of piRNA clusters and reductions in transposition rate are sparse for P -elements, and entirely lacking for other TE families. We therefore harnessed the extensive data on piRNAmediated repression of dysgenic sterility (Marin et al, 2000;Ronsseray et al, 1991Ronsseray et al, , 1996Ronsseray et al, , 1998Simmons et al, 2014Simmons et al, , 2007Simmons et al, , 2012Stuart et al, 2002) (Supplemental Material Table S1, figure S1). Based on these observations, we describe the strength of small-RNA-mediated silencing, R, conferred by maternal genotypes with at least one occupied small-RNA site as…”

Genomic analysis ofPelements in natural populations ofDrosophila melanogaster

“…GD phenotypes were originally proposed to be mediated by repressor proteins encoded by full length P elements or truncated P elements that prevent P element transposition and subsequent DNA damage (Rio, 2002). Other work posits that these phenotypes mostly arise due to RNAi-based repression mediated by piRNAs produced by telomeric P elements and the effects are amplified by RNAs produced by other P elements (Simmons et al, 2014, 2015). More recently, some authors have questioned the classical view that GD phenotypes are caused solely by P elements or whether other factors may be involved (Zakharenko & Ignatenko, 2014; Ignatenko et al, 2015).…”