Endogenous siRNAs and piRNAs derived from transposable elements and genes in the malaria vector mosquito Anopheles gambiae

Abstract

BackgroundThe siRNA and piRNA pathways have been shown in insects to be essential for regulation of gene expression and defence against exogenous and endogenous genetic elements (viruses and transposable elements). The vast majority of endogenous small RNAs produced by the siRNA and piRNA pathways originate from repetitive or transposable elements (TE). In D. melanogaster, TE-derived endogenous siRNAs and piRNAs are involved in genome surveillance and maintenance of genome integrity. In the medically relevant malaria mosquito Anopheles gambiae TEs constitute 12-16% of the genome size. Genetic variations induced by TE activities are known to shape the genome landscape and to alter the fitness in An. gambiae.ResultsHere, using bioinformatics approaches we analyzed the small RNA data sets from 6 libraries formally reported in a previous study and examined the expression of the mixed germline/somatic siRNAs and piRNAs produced in adult An. gambiae females. We characterized a large population of TE-derived endogenous siRNAs and piRNAs, which constitutes 56-60% of the total siRNA and piRNA reads in the analysed libraries. Moreover, we identified a number of protein coding genes producing gene-specific siRNAs and piRNAs that were generally expressed at much lower levels than the TE-associated small RNAs. Detailed sequence analysis revealed that An. gambiae piRNAs were produced by both “ping-pong” dependent (TE-associated piRNAs) and independent mechanisms (genic piRNAs). Similarly to D. melanogaster, more than 90% of the detected piRNAs were produced from TE-associated clusters in An. gambiae. We also found that biotic stress as blood feeding and infection with Plasmodium parasite, the etiological agent of malaria, modulated the expression levels of the endogenous siRNAs and piRNAs in An. gambiae.ConclusionsWe identified a large and diverse set of the endogenously derived siRNAs and piRNAs that share common and distinct aspects of small RNA expression across insect species, and inferred their impact on TE and gene activity in An. gambiae. The TE-specific small RNAs produced by both the siRNA and piRNA pathways represent an important aspect of genome stability and genetic variation, which might have a strong impact on the evolution of the genome and vector competence in the malaria mosquitoes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1436-1) contains supplementary material, which is available to authorized users.

Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes

“…First, it argues strongly that the predominantly germline expression of the piRNA pathway in key model animals (vertebrates, Drosophila, and nematodes) is a derived state, and that "ping-pong" mediated TEsuppression in the soma is likely to be common in other animal phyla, as has recently been shown for arthropods (17), and has very recently been confirmed in two other molluscs (150). Second, it suggests that the TE-derived endo-siRNAs seen in Drosophila and mosquitoes (62,147,(151)(152)(153) are absent from most phyla, and are therefore a relatively recent innovation. Third, the diversity of piRNA profiles we see among organisms-such as the bimodal length distributions of primary piRNAs in the sponge and in "ping-pong' piRNAs in the sea anemone-suggests substantial variation among animals in the details of piRNA biogenesis.…”

The genome ofDrosophila innubilareveals lineage-specific patterns of selection in immune genes

“…However, rates of evolution are mostly consistent There are several other aspects of the host biology that may explain the constrained 441 evolution of the siRNA in D. innubila (Figure 2, 3). siRNA, alongside piRNA have been 442 implicated in transposon regulation as well as viral suppression (Biryukova and Ye 2015). It is 443 possible siRNA has an alternate, TE related role in D. innubila, which may contribute to their low 444 TE content (Figure 1, Supplementary Figure 6).…”

Conserved small nucleotidic elements at the origin of concerted piRNA biogenesis from genes and lncRNAs

“…and AGAP009509 were knocked down. These results obtained by knocking-down independently the three different PIWI class proteins show that AGAP003387 is regulated by the piRNA pathway (19).…”

“…The African malaria vector An. gambiae particularly suits this analysis because first, piRNAs with a ping-pong signature are produced in the ovarian tissue (17)(18)(19) and second, a high proportion of them, 11%, are derived from protein-coding transcripts (17). We here uncover piRNA biogenesis in An.…”