Cytotype regulation inDrosophila melanogaster: synergism between telomeric and non-telomericPelements

Abstract

The X-linked telomeric P elements TP5 and TP6 interact synergistically with non-telomeric P elements to repress hybrid dysgenesis. In this repression, the telomeric P elements exert maternal effects, which, however, are not sufficient to establish synergism with the non-telomeric P elements. Once synergism is established, the capacity to repress dysgenesis in the offspring of a cross persists for at least two generations after removing the telomeric P element from the genotype. At the molecular level, synergism between telomeric and non-telomeric P elements is correlated with effective elimination of P-element mRNA in the germ line. Maternally transmitted mutations in the genes aubergine, piwi and Suppressor of variegation 205 [Su(var)205] block the establishment of synergism between telomeric and non-telomeric P elements, and paternally transmitted mutations in piwi and Su(var)205 disrupt synergism that has already been established. These findings are discussed in terms of a model of cytotype regulation of P elements based on Piwi-interacting RNAs (piRNAs) that are amplified by cycling between sense and antisense species.

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

“…Therefore, mRNAs from nonrepressive P insertions would enhance piRNA production that is initiated by insertions in the X-TAS piRNA cluster, thereby establishing stronger regulation. In support of this model, aub mutations impair both ping-pong amplification ) and the enhanced repression exhibited by maternal genotypes combining TPs with nonrepressive P insertions (Belinco et al 2009;Simmons et al 2012Simmons et al , 2014.…”

“…The requirements for maternal transmission were carefully analyzed by examining the capacity of TP females to repress hybrid dysgenesis in their offspring. In crosses between heterozygous (TP/+) females and P-strain males, ovarian atrophy was approximately equally repressed among the female offspring, regardless of their genotype ( Figure 5A vs. Figure 5B) Simmons et al 2007a;Belinco et al 2009). However, only those female offspring that inherit the TP are themselves able to establish maternal repression (Figure 5B).…”

“…However, significantly-stronger maternal repression is seen when the maternal genotype includes both a TP and additional P elements elsewhere in the genome ( Figure 5B vs. Figure 5C) (Ronsseray et al 1998;Simmons et al 2007aSimmons et al , 2012Simmons et al , 2014Belinco et al 2009). TP-dependent maternal repression, therefore, is epistatically enhanced by additional P-element copies, which in isolation do not confer repression.…”

“…However, recent research has revealed that the piRNA pathway is the molecular basis of cytotype regulation (Reiss et al 2004;Brennecke et al 2008;Jensen et al 2008;Belinco et al 2009;Khurana et al 2011). Indeed, P-cytotype genetics and piRNA-mediated silencing are increasingly synergistic, with classic observations motivating modern molecular experiments and new mechanisms shedding light on old discoveries.…”

“…Maternal heterozygosity for loss-of-function mutations in aub and piwi impairs the repression of P-element activity in offspring (Reiss et al 2004;Simmons et al 2007bSimmons et al , 2010Belinco et al 2009). Similar sensitivity to maternal dosage is also observed with heterochromatin protein 1 (HP1) (Ronsseray et al 1996;Haley et al 2005;Belinco et al 2009;Simmons et al 2010), which promotes the heterochromatic environment required for piRNA cluster transcription (Moshkovich and Lei 2010;Rangan et al 2011).…”