Transposon regulation in Drosophila: piRNA-producing P elements facilitate repression of hybrid dysgenesis by a P element that encodes a repressor polypeptide

Abstract

The transposons of Drosophila melanogaster are regulated by small RNAs that interact with the Piwi family of proteins. These piRNAs are generated from transposons inserted in special loci such as the telomere-associated sequences at the left end of the X chromosome. Drosophila's P transposons can also be regulated by a polypeptide encoded by the KP element, a 1.15-kb-long member of the P family. Using piRNA-generating telomeric P elements (TPs) and repressor-producing transgenic KP elements, we demonstrate a functional connection between these two modes of regulation. By themselves, the TPs partially repress gonadal dysgenesis, a trait caused by rampant P-element activity in the germ line. This repression is manifested as a strictly maternal effect arising from the cytoplasmic transmission of P-specific piRNAs from mother to offspring. The repression is enhanced by genetic interactions between the TPs and other, non-telomeric P elements-a phenomenon attributable to ping-pong amplification of maternal piRNAs. KP elements, like other kinds of non-telomeric P elements, enhance regulation anchored in the TPs. However, with some TPs, the enhanced regulation is manifested as a strictly zygotic effect of the KP element. This effect is seen when the TP has few sequences in common with the KP element, a condition not conducive to ping-pong amplification of piRNAs; it can be attributed to the action of the KP repressor polypeptide. Because the effect is seen only when a TP was present in the mother's genotype, maternally generated P-element piRNAs could facilitate regulation by the KP repressor polypeptide.

Chironomus riparius (Diptera) genome sequencing reveals the impact of minisatellite transposable elements on population divergence

“…; Simmons et al . ) are responsible for hybrid dysgenesis. Hybrids of D. melanogaster strains show elevated rates of mutation, chromosomal rearrangements, male recombination or sterility of females due to gonadal dysfunction (Bingham et al .…”

“…Transposable elements (TEs), which make up a large fraction of most eukaryotic genomes, have been proposed as major driver of genome evolution and attributed an important role in speciation (Kazazian 2004;Werren 2011). The idea that TEs can directly influence hybrid fertility is well supported in Drosophila (Kidwell 1985;Yannopoulos et al 1987;Blumenstiel & Hartl 2005), where three different TEs (P-, I-, and hobo element; Kavi et al 2005;Kofler et al 2015;Simmons et al 2015) are responsible for hybrid dysgenesis. Hybrids of D. melanogaster strains show elevated rates of mutation, chromosomal rearrangements, male recombination or sterility of females due to gonadal dysfunction (Bingham et al 1982;Bucheton et al 1984;Galindo et al 1995).…”

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

“…However, repressor proteins could still play a complementary role to that of piRNAs in regulating P-element activity. A recent study suggests that maternally-deposited piRNAs enhance zygotic regulation by type II repressor proteins (Simmons et al 2015). Furthermore, zygotic repression is beneficial for the offspring of crosses between P element-harboring males and naïve females, where piRNA-mediated regulation is expected to be absent or weak.…”

“…First, they do not focus on strains that exhibit exclusively zygotic repression, meaning that KP-mediated repression and piRNA-mediated repression are confounded. Although weak piRNA-mediated silencing may enhance KP repression (Simmons et al 2015), strong piRNA-mediated silencing would most likely swamp the modest impact of KP elements when found in the same genetic background. The second limitation of many studies of KP-mediated repression is that they often relied on the presence and intensity of a particular restriction fragment size to identify and quantify KP elements.…”

Chironomus riparius(Diptera) genome sequencing reveals the impact of minisatellite transposable elements on population divergence

“…Empirical evidence for the potential involvement of TEs in postzygotic RI comes e.g. from Drosophila, where three different TEs (P-, I-, and hobo element; Kavi et al 2005;Kofler et al 2015;Simmons et al 2015) are responsible for hybrid dysgenesis, which involves elevated rates of mutation, chromosomal rearrangements, illicit recombination in males or sterility of females due to gonadal dysfunction (Bingham et al 1982;Bucheton et al 1984;Galindo et al 1995). Similar TE-mediated hybrid breakdown phenomena have been observed in plants (Martienssen 2010) and vertebrates (Dion-Cote et al 2014).…”