Expression of the Retrotransposon Helena Reveals a Complex Pattern of TE Deregulation in Drosophila Hybrids

Abstract

Transposable elements (TEs), repeated mobile sequences, are ubiquitous in the eukaryotic kingdom. Their mobilizing capacity confers on them a high mutagenic potential, which must be strongly regulated to guarantee genome stability. In the Drosophila germline, a small RNA-mediated silencing system, the piRNA (Piwi-interacting RNA) pathway, is the main responsible TE regulating mechanism, but some stressful conditions can destabilize it. For instance, during interspecific hybridization, genomic stress caused by the shock of two different genomes can lead, in both animals and plants, to higher transposition rates. A recent study in D. buzatii—D. koepferae hybrids detected mobilization of 28 TEs, yet little is known about the molecular mechanisms explaining this transposition release. We have characterized one of the mobilized TEs, the retrotransposon Helena, and used quantitative expression to assess whether its high transposition rates in hybrids are preceded by increased expression. We have also localized Helena expression in the gonads to see if cellular expression patterns have changed in the hybrids. To give more insight into changes in TE regulation in hybrids, we analysed Helena-specific piRNA populations of hybrids and parental species. Helena expression is not globally altered in somatic tissues, but male and female gonads have different patterns of deregulation. In testes, Helena is repressed in F1, increasing then its expression up to parental values. This is linked with a mislocation of Helena transcripts along with an increase of their specific piRNA levels. Ovaries have additive levels of Helena expression, but the ping-pong cycle efficiency seems to be reduced in F1 hybrids. This could be at the origin of new Helena insertions in hybrids, which would be transmitted to F1 hybrid female progeny.

Drosophila Interspecific Hybridization Causes a Deregulation of the piRNA Pathway Genes

“…These results are in concordance with previous studies in hybrids showing high individual and cross heterogeneity in transposition [22] and expression rates [25] of the retrotransposon Osvaldo. In the same way, expression studies on the retrotransposon Helena showed additive patterns of expression in hybrids compared to parental species when using pooled flies in qRT-PCR experiments, while FISH experiments in individual flies showed a more extensive presence of Helena transcripts in F1 hybrids compared to parental species [26]. In the present study, the transcripts of the studied genes were mainly localized in the ovarian nurse cells' cytoplasm in both hybrids and parental species.…”

“…However, ago3 is the only gene that seems to be more expressed in the oocyte of hybrids than of parental species, which might be due to an activation of the piRNA pathway to counteract TE deregulation in hybrids, or to an abnormal localization of the transcripts due to hybrid incompatibilities. Indeed, abnormal distributions of tissue expression were previously reported in Drosophila hybrids [26].…”

“…The combination of divergent Drosophila genomes during hybridization results in a genomic shock characterized, inter alia, by a TE deregulation [22,23,25,26] caused by a failure of TE silencing [20,27,53]. There is limited information linking TE deregulation with expression failures in piRNA pathway genes [27], well-known by their important role in germinal TE regulation.…”

“…Previous work in our laboratory showed that new TE insertions occur in hybrids between the species Drosophila buzzatii and Drosophila koepferae (buzzatii complex, repleta group) [15,22,23], which is likely at the origin of a genome expansion in hybrid females [24]. These TE bursts have been associated with abnormal TE expression patterns, first of the retrotransposons Osvaldo and Helena [25,26] and then in a global transcriptomic study including the whole-genome TEs [27]. Importantly, these studies proved that (i) more TE families are misregulated in F1 ovaries than in the subsequent generations of backcrossed hybrids [27], (ii) TE expression is heterogeneous between hybrid samples from different interspecific crosses [25], and (iii) there are differences in transposition rates even between hybrids of the same cross [22].…”

Stress-driven transposable element de-repression dynamics in a fungal pathogen

“…However, environmental stimuli and stress, in particular, have been shown to trigger epigenetic de-repression of TEs resulting in the activation of insertional mutagenesis (Miousse et al 2015). TE de-repression in response to stress is widely shared across eukaryotes (Bundo et al 2014; Van Meter et al 2014; Voronova et al 2014; Romero-Soriano and Guerreiro 2016; Ryan et al 2016; Zovoilis et al 2016; Huang et al 2017; Hummel et al 2017; Shpyleva et al 2018). De-repression of TEs under stress usually impacts TE transcription levels and can increase transpositional activity (Dubin et al 2018).…”