Whole genome sequencing in Drosophila virilis identifies Polyphemus, a recently activated Tc1-like transposon with a possible role in hybrid dysgenesis

Abstract

BackgroundHybrid dysgenic syndromes in Drosophila have been critical for characterizing host mechanisms of transposable element (TE) regulation. This is because a common feature of hybrid dysgenesis is germline TE mobilization that occurs when paternally inherited TEs are not matched with a maternal pool of silencing RNAs that maintain transgenerational TE control. In the face of this imbalance TEs become activated in the germline and can cause F1 sterility. The syndrome of hybrid dysgenesis in Drosophila virilis was the first to show that the mobilization of one dominant TE, the Penelope retrotransposon, may lead to the mobilization of other unrelated elements. However, it is not known how many different elements contribute and no exhaustive search has been performed to identify additional ones. To identify additional TEs that may contribute to hybrid dysgenesis in Drosophila virilis, I analyzed repeat content in genome sequences of inducer and non-inducer lines.ResultsHere I describe Polyphemus, a novel Tc1-like DNA transposon, which is abundant in the inducer strain of D. virilis but highly degraded in the non-inducer strain. Polyphemus expression is also increased in the germline of progeny of the dysgenic cross relative to reciprocal progeny. Interestingly, like the Penelope element, it has experienced recent re-activation within the D. virilis lineage.ConclusionsHere I present the results of a comprehensive search to identify additional factors that may cause hybrid dysgenesis in D. virilis. Polyphemus, a novel Tc1-like DNA transposon, has recently become re-activated in Drosophila virilis and likely contributes to the hybrid dysgenesis syndrome. It has been previously shown that the Penelope element has also been re-activated in the inducer strain. This suggests that TE co-reactivation within species may synergistically contribute to syndromes of hybrid dysgenesis.

When genomes collide: multiple modes of germline misregulation in a dysgenic syndrome ofDrosophila virilis

“…This analysis reveals two classes of TEs that are enriched in inducer strain 160. Consistent with previous analysis[26,27,31], Penelope and Polyphemus show greater homogeneity among copies in strain 160. This pattern also applies, albeit to a lesser extent, to Helena , Paris, Skippy and the telomeric TART element.…”

“…Furthermore, expression of the Penelope element is elevated in the ovaries and testes of F1 dysgenic progeny that have escaped ablation of the gonad [11]. In addition to the Penelope element, three other elements ( Helena, Paris and Polyphemus [16,27]) are also more abundant in the inducer strain, and these likely contribute to dysgenesis. A complex mode of hybrid dysgenesis, driven jointly by multiple elements, is supported by the fact that some strains of D. virilis lack Penelope piRNAs in the ovary but are “neutral” - capable of preventing dysgenesis when crossed with strain 160 males but also incapable of induction [28].…”

“…To determine whether additional elements to Penelope may contribute to dysgenesis in D. virilis , we performed genome sequencing on both strains 9 (non-inducer) and 160 (inducer). To estimate bulk differences in TE abundance between the two strains, we mapped single end reads against a custom D. virilis TE library (Supplemental 1) that included more TEs than used in the previous analysis of Polyphemus [27]. Relative mapping abundance with BWA-MEM[29], normalized by read number mapping to the reference, is shown in Figure 1A.…”

A Single Gene Causes an Interspecific Difference in Pigmentation inDrosophila

“…This interval mostly contains sequence that is noncoding, but also includes the first exon of isoform-A of Dat . To examine the extent of sequence divergence between the two species in this interval, we generated a multiple sequence alignment of the region using publicly available genome sequences from two strains of D. americana (strain H5 and strain W11; (Fonseca et al 2013)) and two strains of D. virilis (Strain-9 and Strain-160; (Blumenstiel 2014)). By Blasting the candidate region’s sequence from the D. virilis genome to the two D. americana genomes, we recover two and three scaffolds from the H5 and W11 strains, respectively, that cover the ~11kb region in D. virilis .…”

“…Publicly available genome sequences for two D. americana strains (H5 and W11, http://cracs.fc.up.pt/~nf/dame/fasta/; (Fonseca et al 2013)) and two D. virilis strains (Str9: SRX496597, and Str160:SRX496709; (Blumenstiel 2014)) were used to compare the candidate region between the two species. To extract orthologous regions in the D. americana strains, the sequence of the ~11kb candidate region from the D. virilis genome strain (droVir2) was Blasted (BLAST 2.2.28+) against the H5 and W11 genome assemblies.…”