Natural Selection Drives Extremely Rapid Evolution in Antiviral RNAi Genes

Obbard, Darren J.; Jiggins, Francis M.; Halligan, Daniel L.; Little, Tom J.

doi:10.1016/j.cub.2006.01.065

Cited by 267 publications

(310 citation statements)

References 24 publications

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“…It remains unclear whether this reflects an ancient RNAi pathway duplication in the animal lineage that was retained only in insects and/or the fast evolution of certain duplicated sequences within the insect lineage. Although a recent report suggests that D. melanogaster Dcr2 and Ago2 are among the fastest evolving genes in this organism, perhaps as a result of a coevolutionary "arms race" with viral pathogens (Obbard et al 2006).…”

Section: Phylogeny Of Argonaute-piwi Dicer-like and Rdrp Proteinsmentioning

confidence: 99%

On the origin and functions of RNA-mediated silencing: from protists to man

2006

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Double-stranded RNA has been shown to induce gene silencing in diverse eukaryotes and by a variety of pathways. We have examined the taxonomic distribution and the phylogenetic relationship of key components of the RNA interference (RNAi) machinery in members of five eukaryotic supergroups. On the basis of the parsimony principle, our analyses suggest that a relatively complex RNAi machinery was already present in the last common ancestor of eukaryotes and consisted, at a minimum, of one Argonautelike polypeptide, one Piwi-like protein, one Dicer, and one RNAdependent RNA polymerase. As proposed before, the ancestral (but non-essential) role of these components may have been in defense responses against genomic parasites such as transposable elements and viruses. From a mechanistic perspective, the RNAi machinery in the eukaryotic ancestor may have been capable of both small-RNA-guided transcript degradation as well as transcriptional repression, most likely through histone modifications. Both roles appear to be widespread among living eukaryotes and this diversification of function could account for the evolutionary conservation of duplicated Argonaute-Piwi proteins. In contrast, additional RNAi-mediated pathways such as RNA-directed DNA methylation, programmed genome rearrangements, meiotic silencing by unpaired DNA, and miRNA-mediated gene regulation may have evolved independently in specific lineages.

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Section: Phylogeny Of Argonaute-piwi Dicer-like and Rdrp Proteinsmentioning

confidence: 99%

On the origin and functions of RNA-mediated silencing: from protists to man

2006

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“…Given the striking evidence for rapid evolution of Nups, which is possibly driven by intragenomic conflict, we turned our attention to RNAi genes, which are also thought to evolve rapidly due to genomic conflict (Obbard et al 2006(Obbard et al , 2009a. Only 16 out of 23 RNAi genes studied by Obbard et al (2006Obbard et al ( , 2009a and Kolaczkowski et al (2011) were included in the initial D. mauritiana annotation.…”

Section: Signatures Of Positive Selection In D Mauritianamentioning

confidence: 99%

“…Only 16 out of 23 RNAi genes studied by Obbard et al (2006Obbard et al ( , 2009a and Kolaczkowski et al (2011) were included in the initial D. mauritiana annotation. Hence, we manually curated the annotation of the seven missing RNAi genes (AGO2, armi, krimp, AGO3, mael, rhi, and squ).…”

Section: Signatures Of Positive Selection In D Mauritianamentioning

confidence: 99%

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

Nolte¹,

Pandey²,

Kofler³

et al. 2012

Genome Res.

117

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Although it is well understood that selection shapes the polymorphism pattern in Drosophila, signatures of classic selective sweeps are scarce. Here, we focus on Drosophila mauritiana, an island endemic, which is closely related to Drosophila melanogaster. Based on a new, annotated genome sequence, we characterized the genome-wide polymorphism by sequencing pooled individuals (Pool-seq). We show that the interplay between selection and recombination results in a genome-wide polymorphism pattern characteristic for D. mauritiana. Two large genomic regions (>500 kb) showed the signature of almost complete selective sweeps. We propose that the absence of population structure and limited geographic distribution could explain why such pronounced sweep patterns are restricted to D. mauritiana. Further evidence for strong adaptive evolution was detected for several nucleoporin genes, some of which were not previously identified as genes involved in genomic conflict. Since this adaptive evolution is continuing after the split of D. mauritiana and Drosophila simulans, we conclude that genomic conflict is not restricted to short episodes, but rather an ongoing process in Drosophila.

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“…In contrast, and consistent with the antiviral role of Drosophila Ago2, the other domains of this protein display strong evidence of positive selection: they exhibit locally reduced diversity around the gene through selective sweeps, and elevated rates of amino acid substitution (Obbard et al 2006Kolaczkowski et al 2011). We have previously argued that this rapid adaptive evolution may be driven by virus-mediated selection, through the action of viral suppressors of RNAi (Obbard et al 2009), such as those seen in Drosophila C Virus and Drosophila Nora Virus (van Rij et al 2006;van Mierlo et al 2014) .…”

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confidence: 75%

Variation and evolution of the glutamine-rich repeat region of Drosophila Argonaute-2

Palmer

Obbard

2016

Preprint

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RNA interference pathways mediate biological processes through Argonaute-family proteins, which bind small RNAs as guides to silence complementary target nucleic acids . In insects and crustaceans Argonaute-2 silences viral nucleic acids, and therefore acts as a primary effector of innate antiviral immunity. Although the function of the major Argonaute-2 domains, which are conserved across most Argonautefamily proteins, are known, many invertebrate Argonaute-2 homologs contain a glutamine-rich repeat (GRR) region of unknown function at the N-terminus . Here we combine long-read amplicon sequencing of Drosophila Genetic Reference Panel (DGRP) lines with publicly available sequence data from many insect species to show that this region evolves extremely rapidly and is hyper-variable within species. We identify distinct GRR haplotype groups in Drosophila melanogaster, and suggest that one of these haplotype groups has recently risen to high frequency in a North American population. Finally, we use published data from genome-wide association studies of viral resistance in D. melanogaster to test whether GRR haplotypes are associated with survival after virus challenge. We find a marginally significant association with survival after challenge with Drosophila C Virus in the DGRP, but we were unable to replicate this finding using lines from the Drosophila Synthetic Population Resource panel. KEYWORDS

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Natural Selection Drives Extremely Rapid Evolution in Antiviral RNAi Genes

Cited by 267 publications

References 24 publications

On the origin and functions of RNA-mediated silencing: from protists to man

On the origin and functions of RNA-mediated silencing: from protists to man

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

Variation and evolution of the glutamine-rich repeat region of Drosophila Argonaute-2

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