Academic journal article Genetics

Repeated Duplication of Argonaute2 Is Associated with Strong Selection and Testis Specialization in Drosophila

Academic journal article Genetics

Repeated Duplication of Argonaute2 Is Associated with Strong Selection and Testis Specialization in Drosophila

Article excerpt

ARGONAUTE genes are found in almost all eukaryotes, where they play a key role in antiviral immune defense, gene regulation, and genome stability. They perform this diverse range of functions through their role in RNA interference (RNAi) mechanisms, an ancient system of nucleic acid manipulation in which small RNA (sRNA) molecules guide Argonaute proteins to nucleic acid targets through base complementarity (reviewed in Meister 2013). Gene duplication has occurred throughout the evolution of the Argonaute gene family, with ancient duplication events characteristic of some lineages-such as three duplications early in plant evolution (Singh et al. 2015) and multiple expansions and losses throughout the evolution of nematodes (reviewed in Buck and Blaxter 2013) and the Diptera (Lewis et al 2016). After duplication, Argonautes have often undergone functional divergence, involving changes in expression patterns and altered sRNA binding partners (Lu et al. 2011; Leebonoi et al. 2015; Miesen et al. 2015). Duplication early in eukaryotic evolution produced two distinct Argonaute subfamilies, Ago and Piwi, which have since been retained in the vast majority of Metazoa (Cerutti and Casas-Mollano 2006). Members of the Ago subfamily are expressed in both somatic and germline tissue, and variously bind sRNAs derived from host transcripts (miRNAs, endo-siRNAs) or transposable elements (TE endo-siRNAs) and viruses (viRNAs). In contrast, in most vertebrates and arthropods, the Piwi subfamily members are expressed primarily in association with the germline (reviewed in Ross et al. 2014), and bind sRNAs from TEs and host loci (piRNAs), suggesting that the Piwi subfamily specialized to a germline-specific role on the lineages leading to vertebrates and arthropods.

After the early divergence of the Ago and Piwi subfamilies, subsequent duplications gave rise to three Piwi subfamily members [Ago3, Aubergine (Aub), and Piwi] and two Ago subfamily members (Ago1 and Ago2) in Drosophila melanogaster. All three Piwi subfamily genes are associated with the germline and bind piRNAs derived from TEs and other repetitive genomic elements: Ago3 and Aub amplify the piRNA signal through the "Ping-Pong" cycle (reviewed in Luteijn and Ketting 2013), and Piwi suppresses transposition by directing heterochromatin formation (Sienski et al. 2012). These functional differences are associated with contrasting selective regimes, with Aub evolving under positive selection (Kolaczkowski et al. 2011) and more rapidly than Ago3 and Piwi (Obbard et al. 2009a). In contrast, Ago1 binds miRNAs and regulates gene expression by inhibiting translation and marking transcripts for degradation (reviewed in Eulalio et al. 2008). This function imposes strong selective constraint on Ago1, resulting in slow evolution and very few adaptive substitutions (Obbard et al. 2006, 2009a; Kolaczkowski et al. 2011). Finally, Ago2 binds siRNAs from viruses (viRNAs) and TEs (endo-siRNAs), and functions in gene regulation (Wen et al. 2015), dosage compensation (Menon and Meller 2012), and the ubiquitous suppression of viruses (Li et al. 2002; van Rij et al. 2006) and TEs (Chung et al 2008; Czech et al. 2008). Ago2 also evolves under strong positive selection, with frequent selective sweeps (Obbard et al. 2006, 2009a,b, 2011; Kolaczkowski et al. 2011), possibly driven by an arms race with virus-encoded suppressors of RNAi (VSRs) (Obbard et al. 2006; Marques and Carthew 2007; van Mierlo et al. 2014).

In contrast to D. melanogaster, from which most functional knowledge of Ago2 in arthropods is derived, an expansion of Ago2 has been reported in D. pseudoobscura (Hain et al. 2010), providing an opportunity to study how the RNAi pathway evolves after duplication. Given the roles of D. melanogaster Ago2 in antiviral defense (Li et al. 2002; van Rij et al. 2006), TE suppression (Chung et al. 2008; Czech et al. 2008), dosage compensation (Menon and Meller 2012), and gene regulation (Wen et al. 2015), we hypothesized that these D. …

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