Drosophila Interspecific Hybrids Phenocopy piRNA-Pathway Mutants

Daniel A Barbash,Nathaniel B Edelman,Mohamed A F Noor,Erin S Kelleher

doi:10.1371/journal.pbio.1001428

Abstract

Author SummaryEukaryotic genomes contain large quantities of transposable elements (TEs), short self-replicating DNA sequences that can move within the genome. The selfish replication of TEs has potentially drastic consequences for the host, such as disruption of gene function, induction of sterility, and initiation or exacerbation of some cancers. Like the adaptive immune system that defends our bodies against pathogens, the Piwi-interacting RNA (piRNA) pathway defends animal genomes against the harmful effects of TEs. Fundamental to piRNA-mediated defense is the production of small noncoding RNAs that act like antibodies to target replicating TEs for destruction by piRNA-effector proteins. piRNAs are expected to diverge rapidly between species in response to genome infection by increasingly disparate TEs. Here, we tested this hypothesis by examining how differences in piRNAs between two species of fruit fly relate to TE “immunity” in their hybrid offspring. Because piRNAs are maternally deposited, we expected excessive replication of paternal TEs in hybrids. Surprisingly, we observe increased activity of both maternal and paternal TEs, together with defects in piRNA production that are reminiscent of piRNA effector-protein mutants. Our observations reveal that piRNA effector-proteins do not function properly in hybrids, and we propose that adaptive evolution among piRNA effector-proteins contributes to host genome defense and leads to the functional incompatibilities that we observe in hybrids.

Highlights

Transposable elements (TEs) are ubiquitous, mobile genetic parasites that often are exceptionally deleterious to their hosts
Our observations reveal that Piwi-interacting RNA (piRNA) effector-proteins do not function properly in hybrids, and we propose that adaptive evolution among piRNA effector-proteins contributes to host genome defense and leads to the functional incompatibilities that we of the same Drosophila species [22,23,24,25]
Hybrid dysgenesis occurs when the paternal but not maternal strain carries active members of a transposable element (TE) family [26,27,28]. piRNAs derived from the dysgenic TE family are rare or absent in the maternal cytotype because active TE copies are found exclusively in the paternal genome

Summary

Introduction

Transposable elements (TEs) are ubiquitous, mobile genetic parasites that often are exceptionally deleterious to their hosts. Unrestricted TE propagation, is associated with severe pathologies including tumorigenesis, tumor progression, gonadal atrophy, and sterility [3,4,5,6]. Despite these costs, many TE families are extraordinarily successful parasites: they achieve high copy numbers within host genomes [7,8] and can invade novel hosts through horizontal transfer [9,10,11,12]. Recent studies have revealed that in metazoan germlines, the Piwi-interacing RNA pathway (piRNA pathway) acts as a genomic immune system, mediating transcriptional and post-transcriptional silencing of endogenous and invasive TEs (reviewed in [13,14]). The mechanism of piRNA-mediated silencing is best understood in Drosophila, where it is defined by short, antisense, TE-derived RNAs (piRNAs, 23–29 nt) that are found in complexes with three Piwi-clade Argonaute proteins: Piwi, Aubergine (Aub), and Argonaute-3 (Ago3) [17]

Methods

Results

Discussion

Conclusion