Increased production of piRNAs from euchromatic clusters and genes in Anopheles gambiae compared with Drosophila melanogaster

Abstract

BackgroundSpecific genomic loci, termed Piwi-interacting RNA (piRNA) clusters, manufacture piRNAs that serve as guides for the inactivation of complementary transposable elements (TEs). The piRNA pathway has been accurately detailed in Drosophila melanogaster, while it remains poorly examined in other insects. This pathway is increasingly recognized as critical for germline development and reproduction. Understanding of the piRNA functions in mosquitoes could offer an opportunity for disease vector control by the reduction of their reproductive potential.ResultsTo analyze the similarities and differences in this pathway between Drosophila and mosquito, we performed an in-depth analysis of the genomic loci producing piRNAs and their targets in the African malaria vector Anopheles gambiae. We identified 187 piRNA clusters in the An. gambiae genome and 155 piRNA clusters in the D. melanogaster genome. We demonstrate that many more piRNA clusters in the mosquito compared with the fruit fly are uni-directionally transcribed and are located outside pericentromeric heterochromatin. About 11 % of the An. gambiae piRNA population map to gene transcripts. This is a noticeable increase compared with the ~6 % of the piRNA population mapped to genes in D. melanogaster. A subset of the piRNA-enriched genes in An. gambiae has functions related to reproduction and development. At least 24 and 65 % of the mapped piRNAs correspond to genomic TE sequences in An. gambiae and D. melanogaster, respectively. DNA transposons and non-LTR retrotransposons are more abundant in An. gambiae, while LTR retrotransposons are more abundant in D. melanogaster. Yet, piRNAs predominantly target LTR retrotransposons in both species, which may point to a distinct feature of these elements compared to the other classes of TEs concerning their silencing by the piRNA pathway.ConclusionsHere, we demonstrate that piRNA-producing loci have more ubiquitous distribution in the An. gambiae genome than in the genome of D. melanogaster. Also, protein-coding genes have an increased role in production of piRNAs in the germline of this mosquito. Genes involved in germline and embryonic development of An. gambiae generate a substantial portion of piRNAs, suggesting a role of the piRNA pathway in the epigenetic regulation of the reproductive processes in the African malaria vector.Electronic supplementary materialThe online version of this article (doi:10.1186/s13072-015-0041-5) contains supplementary material, which is available to authorized users.

piRNA‐19128 regulates spermatogenesis by silencing of KIT in chicken

“…piRNAs differ from miRNAs with respect to length, lack of conserved sequences, and increased complexity. Length of piRNAs varies in different species and different stage . Result of piRNA length distribution analysis performed in the present study suggested that the length of chicken piRNAs was 23‐30 nt in PGCs and SSCs cells.…”

“…The length of mouse piRNAs is 23-31 nt, 5 that of zebrafish piRNAs is 26-30 nt, 6 and that of D. melanogaster piRNAs is 23-29 nt. 7 In chicken, it remains unclear whether chicken piRNAs are produced through the ping-pong pathway and what the length distribution of piRNAs.Results of small RNA sequencing have shown that piRNAs promote germline stem cell proliferation during early chick development. 8 A study involving CLIP-seq showed that proper turnover of some key piRNA targets was essential for sperm formation.…”

piRNAs and their diverse roles: a transposable element‐driven tactic for gene regulation?

“…Although PIWI protein mutations in the mouse disrupt TE silencing, the relatively minor fraction of piRNAs matching transposons represents one of the major puzzles in the field. A fair proportion (;24%) of piRNAs correspond to TE sequences in the mosquito Anopheles gambiae, as shown in a recent study by George et al (9). However, a more detailed annotation of the Anopheles genome and TE library, as well as a characterization of the clusters are awaited to conclude whether insect piRNA sequences are, in general, high in TEs.…”

“…Afair proportion (∼24%) of piRNAs correspond to TE sequences in the mosquito Anopheles gambiae, as showninarecent studybyGeorge et al . (9). However, a more detailed annotation of the Anopheles genome and TE library, as well as a characterization of the clusters are awaited to conclude whether insect piRNA sequences are, in general, high in TEs.…”

Trapping a somatic endogenous retrovirus into a germline piRNA cluster immunizes the germline against further invasion

“…Using this approach, we identified a new ZAM insertion that mapped to a R1 element sequence found at multiple locations within cluster 9 [29], a dual-strand piRNA cluster located next to the X chromosome centromere (Fig. S4F).…”