Diversity of P-element piRNA production among M' and Q strains and its association with P-M hybrid dysgenesis in Drosophila melanogaster

Abstract

BackgroundTransposition of P elements in the genome causes P–M hybrid dysgenesis in Drosophila melanogaster. For the P strain, the P–M phenotypes are associated with the ability to express a class of small RNAs, called piwi-interacting small RNAs (piRNAs), that suppress the P elements in female gonads. However, little is known about the extent to which piRNAs are involved in the P–M hybrid dysgenesis in M′ and Q strains, which show different abilities to regulate the P elements from P strains.ResultsTo elucidate the molecular basis of the suppression of paternally inherited P elements, we analyzed the mRNA and piRNA levels of P elements in the F1 progeny between males of a P strain and nine-line females of M′ or Q strains (M′ or Q progenies). M′ progenies showed the hybrid dysgenesis phenotype, while Q progenies did not. Consistently, the levels of P-element mRNA in both the ovaries and F1 embryos were higher in M′ progenies than in Q progenies, indicating that the M′ progenies have a weaker ability to suppress P-element expression. The level of P-element mRNA was inversely correlated to the level of piRNAs in F1 embryos. Importantly, the M′ progenies were characterized by a lower abundance of P-element piRNAs in both young ovaries and F1 embryonic bodies. The Q progenies showed various levels of piRNAs in both young ovaries and F1 embryonic bodies despite all of the Q progenies suppressing P-element transposition in their gonad.ConclusionsOur results are consistent with an idea that the level of P-element piRNAs is a determinant for dividing strain types between M′ and Q and that the suppression mechanisms of transposable elements, including piRNAs, are varied between natural populations.Electronic supplementary materialThe online version of this article (10.1186/s13100-017-0096-x) contains supplementary material, which is available to authorized users.

Har-P, a short P-element variant, weaponizes P-transposase to severely impair Drosophila development

“…Although this dispersion of de novo P-elements in HISR lines’ genomes stymied our goal to pinpoint a particular Har locus strongly inducing GD, we next cloned and sequenced genomic PCR amplicons of all P -elements from the various P -element-containing strains. By using a single oligonucleotide that primes from both the 5' and 3' Terminal Inverted Repeats (TIRs), we amplified full-length P -elements as well as several additional truncation variants (Figure 5A) that have been missed in other genomic PCR assays using internal primers (Wakisaka et al, 2017). The most abundant variant accounting for more P -element copies in OreR-MOD and OreR-TK strains compared to Har were the ‘ KP ’ variant shown to encode a dominant negative protein that inhibits full-length P -transposase activity (Jackson et al, 1988; Simmons et al, 1990) (Figure 5A–5C), thus explaining the innocuous accumulation of these P -element variants in these OreR strains.…”

“…Between fertility and complete sterility lies a spectrum of GD induction variation amongst different strain crosses that may be attributed to differential P -element copy numbers in different strain genomes (Anxolabéhère et al, 1985; Bergman et al, 2017; Biémont et al, 1990; Bingham et al, 1982; Boussy et al, 1988; Kidwell et al, 1981; Ronsseray et al, 1989; Srivastav and Kelleher, 2017; Yoshitake et al, 2018), and capacity to generate piRNAs (Wakisaka et al, 2017). In addition, there are many non-autonomous P -element variants that can be mobilized by P -transposases, including very short elements from the pi[2] strain (Bingham et al, 1982; O'Hare and Rubin, 1983) that actually assemble in vitro with the P -transposase tetramer complex >100X more efficiently than the full-length P -element (Tang et al, 2007).…”

Har-P, ashortP-element variant, weaponizesP-transposase to severely impairDrosophiladevelopment

“…By using a single oligonucleotide that primes from both the 5’ and 3’ Terminal Inverted Repeats (TIRs), we amplified full-length P -elements as well as several additional truncation variants (Fig. 5A) that have been missed in other genomic PCR assays using internal primers (Wakisaka et al, 2017). The most abundant variant accounting for more P -element copies in OreR-MOD and OreR-TK strains compared to Har were the “ KP ” variant shown to encode a dominant negative protein that inhibits full-length P -transposase activity (Jackson et al, 1988; Simmons et al, 1990) (Fig.…”

“…When a P -element truncates to a ∼630bp Har-P variant, this non-autonomous variant dominates as the main mobilizing P -element during a dysgenic cross to induce strong GD. Therefore previous studies examining GD variability across other Drosophila strains and isolates may now be explained by whether these genomes contain both full length and very short P -elements (Bergman et al, 2017; Kozeretska et al, 2018; Ronsseray et al, 1989; Srivastav and Kelleher, 2017; Wakisaka et al, 2017; Yoshitake et al, 2018).…”

“…Between fertility and complete sterility lies a spectrum of GD induction variation amongst different strain crosses that may be attributed to differential P -element copy numbers in different strain genomes (Anxolabehere et al, 1985; Bergman et al, 2017; Biemont et al, 1990; Bingham et al, 1982; Boussy et al, 1988; Kidwell et al, 1981; Ronsseray et al, 1989; Srivastav and Kelleher, 2017; Yoshitake et al, 2018), and capacity to generate piRNAs (Wakisaka et al, 2017). In addition, there are many non-autonomous P -element variants that can be mobilized by P -transposases, including very short elements from the pi [ 2 ] strain (Bingham et al, 1982; O’Hare and Rubin, 1983) that actually assemble in vitro with the P -transposase tetramer complex >100X more efficiently than the full-length P -element (Tang et al, 2007).…”