Developmental piRNA profiles of the invasive vector mosquito Aedes albopictus

Peiwen Liu,Yunqiao Dong,Yang Wu,Jinbao Gu,Santhosh Puthiyakunnon,Xiao-Guang Chen

doi:10.1186/s13071-016-1815-8

Peiwen Liu, Yunqiao Dong + Show 4 more

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https://doi.org/10.1186/s13071-016-1815-8

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Abstract

BackgroundIn eukaryotic organisms, Piwi-interacting RNAs (piRNAs) control the activities of mobile genetic elements and ensure genome maintenance. Recent evidence indicates that piRNAs are involved in multiple biological pathways, including transcriptional regulation of protein-coding genes, sex determination and even interactions between host and pathogens. Aedes albopictus is a major invasive species that transmits a number of viral diseases in humans. Ae. albopictus has the largest genome and the highest abundance of repetitive sequences when compared with members that belong to Culicidae with a published genome. Analysis of piRNA profiles will provide a developmental and evolutionary perspective on piRNAs in Ae. albopictus.MethodspiRNAs were identified and characterized during the development of Ae. albopictus, and piRNA expression patterns in adult males and females as well as sugar-fed females and blood-fed females were compared.ResultsOur results reveal that, despite the large genome size of Ae. albopictus, the piRNA pool of Ae. albopictus (1.2 × 107) is smaller than those of Aedes aegypti (1.7 × 107) and Drosophila melanogaster (1.6 × 107). In Ae. albopictus, piRNAs displayed the highest abundance at the embryo stage and the lowest abundance at the pupal stage. Approximately 50 % of the piRNAs mapped to intergenic regions with no known functions. Approximately 30 % of the piRNAs mapped to repetitive elements, and 77.69 % of these repeat-derived piRNAs mapped to Class I TEs; 45.42 % of the observed piRNA reads originated from piRNA clusters, and most of the top 10 highest expressed piRNA clusters and 100 highest expressed piRNAs from each stage displayed biased expression patterns across the developmental stages. All anti-sense-derived piRNAs displayed a preference for uridine at the 5′ end; however, the sense-derived piRNAs showed adenine bias at the tenth nucleotide position and a typical ping-pong signature, suggesting that the biogenesis of piRNAs was conserved throughout development. Our results also show that 962 piRNAs displayed sex-biased expression, and 522 piRNAs showed higher expression in the blood-fed females than in the sugar-fed females.ConclusionsOur results suggest that piRNAs, aside from silencing transposable elements in Ae. albopictus, may have a role in other biological pathways.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1815-8) contains supplementary material, which is available to authorized users.

Highlights

In eukaryotic organisms, P-element induced wimpy testis (Piwi)-interacting RNAs control the activities of mobile genetic elements and ensure genome maintenance
In Drosophila melanogaster, biogenesis of Piwi-interacting RNAs (piRNAs) requires three PIWI proteins: P-element induced wimpy testis (Piwi), Aubergine (Aub) and Argonaute 3 (Ago3) [13, 14]. piRNAs are mainly generated from distinct chromosomal region that are referred to as piRNA clusters
Our results showed that the sexbiased piRNAs and highly expressed piRNAs in the sugar-fed adult females were primarily derived from an intergenic region; this finding leads us to propose a potential role for intergenic piRNAs in transposon control in gonads and early embryos

Summary

Introduction

Piwi-interacting RNAs (piRNAs) control the activities of mobile genetic elements and ensure genome maintenance. PiRNAs differ from other small regulatory non-coding RNAs like (ncRNAs) such as siRNAs and miRNAs in many respects They are processed from unidirectional single-stranded RNA precursors transcribed from intergenic repetitive elements, transposons, or large piRNA clusters and are produced independently of either Drosha or Dicer [10,11,12]. The 5′ ends of precursor piRNAs might be generated by cleavage with a Phospholipase D-like protein, nuclease Zucchini (Zuc) [15,16,17] These 5′ ends trimmed precursor piRNAs are loaded onto PIWI proteins and are further trimmed from their 3′ end to the size of mature piRNAs by an unknown 3–5′ exonuclease. Ago3bound sense piRNAs are enriched for adenosine at position 10 (10-A) [22], and Aub-associated antisense and Ago3-associated sense piRNAs often overlap by precisely 10 nt from their 5′ ends [21, 23, 24]

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