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      Developmental piRNA profiles of the invasive vector mosquito Aedes albopictus

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          Abstract

          Background

          In 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.

          Methods

          piRNAs 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.

          Results

          Our results reveal that, despite the large genome size of Ae. albopictus, the piRNA pool of Ae. albopictus (1.2 × 10 7) is smaller than those of Aedes aegypti (1.7 × 10 7) and Drosophila melanogaster (1.6 × 10 7). 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.

          Conclusions

          Our results suggest that piRNAs, aside from silencing transposable elements in Ae. albopictus, may have a role in other biological pathways.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-016-1815-8) contains supplementary material, which is available to authorized users.

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          Most cited references69

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          Evolutionary genetics of invasive species

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            A distinct small RNA pathway silences selfish genetic elements in the germline.

            In the Drosophila germline, repeat-associated small interfering RNAs (rasiRNAs) ensure genomic stability by silencing endogenous selfish genetic elements such as retrotransposons and repetitive sequences. Whereas small interfering RNAs (siRNAs) derive from both the sense and antisense strands of their double-stranded RNA precursors, rasiRNAs arise mainly from the antisense strand. rasiRNA production appears not to require Dicer-1, which makes microRNAs (miRNAs), or Dicer-2, which makes siRNAs, and rasiRNAs lack the 2',3' hydroxy termini characteristic of animal siRNA and miRNA. Unlike siRNAs and miRNAs, rasiRNAs function through the Piwi, rather than the Ago, Argonaute protein subfamily. Our data suggest that rasiRNAs protect the fly germline through a silencing mechanism distinct from both the miRNA and RNA interference pathways.
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              A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila.

              In Drosophila, repeat-associated small interfering RNAs (rasiRNAs) are produced in the germ line by a Dicer-independent pathway and function through the PIWI subfamily of Argonautes to ensure silencing of retrotransposons. We sequenced small RNAs associated with the PIWI subfamily member AGO3. Although other members of PIWI, Aubergine (Aub) and Piwi, associated with rasiRNAs derived mainly from the antisense strand of retrotransposons, AGO3-associated rasiRNAs arose mainly from the sense strand. Aub- and Piwi-associated rasiRNAs showed a strong preference for uracil at their 5' ends, and AGO3-associated rasiRNAs showed a strong preference for adenine at nucleotide 10. Comparisons between AGO3- and Aub-associated rasiRNAs revealed pairs of rasiRNAs showing complementarities in their first 10 nucleotides. Aub and AGO3 exhibited Slicer activity in vitro. These data support a model in which formation of a 5' terminus within rasiRNA precursors is guided by rasiRNAs originating from transcripts of the other strand in concert with the Slicer activity of PIWI.
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                Author and article information

                Contributors
                irvingliu@163.com
                dongyunqiao@126.com
                daipeng217@126.com
                santhoshpk73@hotmail.com
                lxqx.young@qq.com
                xgchen2001@hotmail.com
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                29 September 2016
                29 September 2016
                2016
                : 9
                : 524
                Affiliations
                [1 ]Department of Pathogen Biology, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou, Guangdong 510515 China
                [2 ]Reproductive Medical Centre of Guangdong Women and Children Hospital, Guangzhou, Guangdong 511442 China
                Article
                1815
                10.1186/s13071-016-1815-8
                5041409
                27686069
                22bbca48-ead5-4d8b-83ba-d6794a89a005
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 11 August 2016
                : 22 September 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 81371846
                Award ID: 81420108024
                Award Recipient :
                Funded by: Scientific and Technological Program of Guangdong
                Award ID: 2013B051000052
                Award Recipient :
                Funded by: International Cooperation Program of Guangzhou
                Award ID: 2013J4500016
                Award Recipient :
                Funded by: Pearl River S and T Nova Program of Guangzhou
                Award ID: 2014J2200032
                Award Recipient :
                Funded by: Research Team Program of Natural Science Foundation of Guangdong
                Award ID: 2014A030312016
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                aedes albopictus,piwi-interacting rnas,transposable elements
                Parasitology
                aedes albopictus, piwi-interacting rnas, transposable elements

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