Dataset Information

Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti.

ABSTRACT: RNA silencing, or RNA interference (RNAi) in metazoans mediates development, reduces viral infection and limits transposon mobility. RNA silencing involves 21-30 nucleotide RNAs classified into microRNA (miRNA), exogenous and endogenous small interfering RNAs (siRNA), and Piwi-interacting RNA (piRNA). Knock-out, silencing and mutagenesis of genes in the exogenous siRNA (exo-siRNA) regulatory network demonstrate the importance of this RNAi pathway in antiviral immunity in Drosophila and mosquitoes. In Drosophila, genes encoding components for processing exo-siRNAs are among the fastest evolving 3% of all genes, suggesting that infection with pathogenic RNA viruses may drive diversifying selection in their host. In contrast, paralogous miRNA pathway genes do not evolve more rapidly than the genome average. Silencing of exo-siRNA pathway genes in mosquitoes orally infected with arboviruses leads to increased viral replication, but little is known about the comparative patterns of molecular evolution among the exo-siRNA and miRNA pathways genes in mosquitoes. We generated nearly complete sequences of all exons of major miRNA and siRNA pathway genes dicer-1 and dicer-2, argonaute-1 and argonaute-2, and r3d1 and r2d2 in 104 Aedes aegypti mosquitoes collected from six distinct geographic populations and analyzed their genetic diversity. The ratio of replacement to silent amino acid substitutions was 1.4 fold higher in dicer-2 than in dicer-1, 27.4 fold higher in argonaute-2 than in argonaute-1 and similar in r2d2 and r3d1. Positive selection was supported in 32% of non-synonymous sites in dicer-1, in 47% of sites in dicer-2, in 30% of sites in argonaute-1, in all sites in argonaute-2, in 22% of sites in r3d1 and in 55% of sites in r2d2. Unlike Drosophila, in Ae. aegypti, both exo-siRNA and miRNA pathway genes appear to be undergoing rapid, positive, diversifying selection. Furthermore, refractoriness of mosquitoes to infection with dengue virus was significantly positively correlated for nucleotide diversity indices in dicer-2.

SUBMITTER: Bernhardt SA

PROVIDER: S-EPMC3448618 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti.

Bernhardt Scott A SA Simmons Mark P MP Olson Ken E KE Beaty Barry J BJ Blair Carol D CD Black William C WC

PloS one 20120921 9

RNA silencing, or RNA interference (RNAi) in metazoans mediates development, reduces viral infection and limits transposon mobility. RNA silencing involves 21-30 nucleotide RNAs classified into microRNA (miRNA), exogenous and endogenous small interfering RNAs (siRNA), and Piwi-interacting RNA (piRNA). Knock-out, silencing and mutagenesis of genes in the exogenous siRNA (exo-siRNA) regulatory network demonstrate the importance of this RNAi pathway in antiviral immunity in Drosophila and mosquitoe ...[more]

PMID: 23028502

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Project description:Female Aedes aegypti mosquitoes impose a severe global public health burden as primary vectors of multiple viral and parasitic pathogens. Under optimal environmental conditions, Aedes aegypti females have access to human hosts that provide blood proteins for egg development, conspecific males that provide sperm for fertilization, and freshwater that serves as an egg-laying substrate suitable for offspring survival. As global temperatures rise, Aedes aegypti females are faced with climate challenges, like intense droughts and intermittent precipitation, which create unpredictable and suboptimal conditions for the egg-laying step of their reproductive cycle. Aedes aegypti mosquitoes nonetheless show remarkable reproductive resilience, but how they achieve this is unknown. Here we show that under drought-like conditions simulated in the laboratory, mated, blood-fed Aedes aegypti females carrying mature eggs retain them in their ovaries for extended periods, while maintaining the viability of these eggs until they can be deposited in freshwater. Using transcriptomic and proteomic profiling of Aedes aegypti ovaries, we identify two previously uncharacterized genes – here named tweedledee and tweedledum – that show ovary-enriched, temporally-restricted expression during egg retention. These genes are mosquito-specific, linked within a syntenic locus, and rapidly evolving under positive selection, raising the possibility that they serve an adaptive function. Using loss-of-function mutagenesis to disrupt both genes, we show that, tweedledee and tweedledum, which encode secreted proteins, are specifically required for extended retention of viable eggs, such as during intermittent precipitation or drought. These results highlight an elegant example of taxon-restricted genes at the heart of an important adaptation that equips Aedes aegypti females with “insurance” to, when contextually appropriate, flexibly extend their reproductive sequence without losing reproductive capacity, thus allowing this species to exploit diverse and unpredictable/chaotic/changing habitats.

Dataset Information

Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti.

Publications

Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti.

Similar Datasets

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