Duplication and Diversification of Dipteran Argonaute Genes, and the Evolutionary Divergence of Piwi and Aubergine

Lewis, Samuel H.; Salmela, Heli; Obbard, Darren J.

doi:10.1093/gbe/evw018

Cited by 107 publications

(130 citation statements)

References 78 publications

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“…piRNAs are associated with PIWI-family Argonautes, which have undergone similar duplications. Piwi has duplicated in L. migratoria , the centipede Strigamia maritima , the pea aphid Acyrthosiphon pisum 18 , the mosquito Aedes aegypti 24 , and flies (generating piwi and aubergine 19 ). All species harbour a single copy of ago3 , which encodes the other PIWI-family Argonaute associated with piRNAs, except for A. pisum which has two ago3 genes.…”

Section: Resultsmentioning

confidence: 99%

Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

Lewis¹,

Quarles²,

Yang³

et al. 2017

Nat Ecol Evol

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253

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Summary Paragraph In animals, small RNA molecules termed PIWI-interacting RNAs (piRNAs) silence transposable elements (TEs), protecting the germline from genomic instability and mutation. piRNAs have been detected in the soma in a few animals, but these are believed to be specific adaptations of individual species. Here, we report that somatic piRNAs were likely present in the ancestral arthropod more than 500 million years ago. Analysis of 20 species across the arthropod phylum suggests that somatic piRNAs targeting TEs and mRNAs are common among arthropods. The presence of an RNA-dependent RNA polymerase in chelicerates (horseshoe crabs, spiders, scorpions) suggests that arthropods originally used a plant-like RNA interference mechanism to silence TEs. Our results call into question the view that the ancestral role of the piRNA pathway was to protect the germline and demonstrate that small RNA silencing pathways have been repurposed for both somatic and germline functions throughout arthropod evolution.

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Section: Resultsmentioning

confidence: 99%

Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

Lewis¹,

Quarles²,

Yang³

et al. 2017

Nat Ecol Evol

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243

253

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“…This becomes apparent in many aspects: (i) The composition of piRNA pathway components differs between Drosophila and mosquitoes (Fig 1). Notably, the PIWI gene family, which lies at the heart of the piRNA pathway, has undergone expansion in both Aedes and Culex mosquitoes [40,41]. In addition, the recent annotations of mosquito genomes do not contain orthologs for all the established factors involved in Drosophila piRNA biogenesis and function [42].…”

Section: Small Rnas In Arboviral Infectionsmentioning

confidence: 99%

“…The Cx . quinquefasciatus PIWI gene family, however, has undergone expansion to seven members [40,41]. …”

Section: Vpirnas In Other Host Speciesmentioning

confidence: 99%

PIWIs Go Viral: Arbovirus-Derived piRNAs in Vector Mosquitoes

2016

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Vector mosquitoes are responsible for transmission of the majority of arthropod-borne (arbo-) viruses. Virus replication in these vectors needs to be sufficiently high to permit efficient virus transfer to vertebrate hosts. The mosquito immune response therefore is a key determinant for arbovirus transmission. Mosquito antiviral immunity is primarily mediated by the small interfering RNA pathway. Besides this well-established antiviral machinery, the PIWI-interacting RNA (piRNA) pathway processes viral RNA into piRNAs. In recent years, significant progress has been made in characterizing the biogenesis and function of these viral piRNAs. In this review, we discuss these developments, identify knowledge gaps, and suggest directions for future research.

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“…Ago2 and other RNAi genes have undergone frequent expansions in different eukaryotic lineages (Mukherjee et al 2013;Lewis et al 2016) and have been shown to switch between ubiquitous and germline-or ovaryspecific functions in isolated species. This study provides evidence for the evolution of a new testis-specific RNAi function and suggests that positive selection may act on young paralogs to drive the rapid evolution of novel RNAi mechanisms across the eukaryotes.…”

Section: Prospects For Novel Functions During the Evolution Of Rnaimentioning

confidence: 99%

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Lewis

Webster

Salmela

et al. 2016

Preprint

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Argonaute2 (Ago2) is a rapidly evolving nuclease in the Drosophila melanogaster RNA interference (RNAi) pathway that targets viruses and transposable elements in somatic tissues. Here we reconstruct the history of Ago2 duplications across the D. obscura group and use patterns of gene expression to infer new functional specialization. We show that some duplications are old, shared by the entire species group, and that losses may be common, including previously undetected losses in the lineage leading to D. pseudoobscura. We find that while the original (syntenic) gene copy has generally retained the ancestral ubiquitous expression pattern, most of the novel Ago2 paralogs have independently specialized to testis-specific expression. Using population genetic analyses, we show that most testis-specific paralogs have significantly lower genetic diversity than the genome-wide average. This suggests recent positive selection in three different species, and model-based analyses provide strong evidence of recent hard selective sweeps in or near four of the six D. pseudoobscura Ago2 paralogs. We speculate that the repeated evolution of testis specificity in obscura group Ago2 genes, combined with their dynamic turnover and strong signatures of adaptive evolution, may be associated with highly derived roles in the suppression of transposable elements or meiotic drive. Our study highlights the lability of RNAi pathways, even within well-studied groups such as Drosophila, and suggests that strong selection may act quickly after duplication in RNAi pathways, potentially giving rise to new and unknown RNAi functions in nonmodel species. KEYWORDS Argonaute; RNAi; Drosophila; duplication; testis A RGONAUTE 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 . 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) ...

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Duplication and Diversification of Dipteran Argonaute Genes, and the Evolutionary Divergence of Piwi and Aubergine

Cited by 107 publications

References 78 publications

Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

PIWIs Go Viral: Arbovirus-Derived piRNAs in Vector Mosquitoes

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

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