Abstract
Almost all eukaryotes have transposable elements (TEs) against which they have developed defense mechanisms. In the Drosophila germline, the main transposable element (TE) regulation pathway is mediated by specific Piwi-interacting small RNAs (piRNAs). Nonetheless, for unknown reasons, TEs sometimes escape cellular control during interspecific hybridization processes. Because the piRNA pathway genes are involved in piRNA biogenesis and TE control, we sequenced and characterized nine key genes from this pathway in Drosophila buzzatii and Drosophila koepferae species and studied their expression pattern in ovaries of both species and their F1 hybrids. We found that gene structure is, in general, maintained between both species and that two genes—armitage and aubergine—are under positive selection. Three genes—krimper, methyltransferase 2, and zucchini—displayed higher expression values in hybrids than both parental species, while others had RNA levels similar to the parental species with the highest expression. This suggests that the overexpression of some piRNA pathway genes can be a primary response to hybrid stress. Therefore, these results reinforce the hypothesis that TE deregulation may be due to the protein incompatibility caused by the rapid evolution of these genes, leading to a TE silencing failure, rather than to an underexpression of piRNA pathway genes.
Highlights
Transposable elements (TEs) are mobile genetic units that are interspersed throughout the genomes of almost all eukaryotes, often occupying significant fractions of the genome of their hosts
(piRNA) pathway acts by silencing transposable elements (TEs) transcriptionally and post-transcriptionally through sequence homology between Piwi-interacting small RNAs (piRNAs) and TEs [3,4,5]. piRNA biogenesis starts when long piRNA precursors are transcribed from specific genomic piRNA clusters and cleaved to produce primary piRNAs [4]
Our results revealed that some of the piRNA pathway genes were deregulated in the gonads of our Drosophila hybrids
Summary
Transposable elements (TEs) are mobile genetic units that are interspersed throughout the genomes of almost all eukaryotes, often occupying significant fractions of the genome of their hosts. 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 in a global transcriptomic study including the whole-genome TEs [27]. Our results revealed that some of the piRNA pathway genes were deregulated in the gonads of our Drosophila hybrids This expression deregulation together with protein incompatibility—due to the rapid evolution of these genes—is likely to be related to the TE silencing failure in cross-species hybrids observed in previous studies [22,23]
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