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The germline of the malaria mosquito produces abundant miRNAs, endo-siRNAs, piRNAs and 29-nt small RNAs.

Castellano, Leandro; Rizzi, Ermanno; Krell, Jonathan; Di Cristina, Manlio; Galizi, Roberto; Mori, Ayako; Tam, Janis; De Bellis, Gianluca; Stebbing, Justin; Crisanti, Andrea; Nolan, Tony

The germline of the malaria mosquito produces abundant miRNAs, endo-siRNAs, piRNAs and 29-nt small RNAs. Thumbnail


Authors

Leandro Castellano

Ermanno Rizzi

Jonathan Krell

Manlio Di Cristina

Ayako Mori

Janis Tam

Gianluca De Bellis

Justin Stebbing

Andrea Crisanti

Tony Nolan



Abstract

BACKGROUND: Small RNAs include different classes essential for endogenous gene regulation and cellular defence against genomic parasites. However, a comprehensive analysis of the small RNA pathways in the germline of the mosquito Anopheles gambiae has never been performed despite their potential relevance to reproductive capacity in this malaria vector. RESULTS: We performed small RNA deep sequencing during larval and adult gonadogenesis and find that they predominantly express four classes of regulatory small RNAs. We identified 45 novel miRNA precursors some of which were sex-biased and gonad-enriched , nearly doubling the number of previously known miRNA loci. We also determine multiple genomic clusters of 24-30 nt Piwi-interacting RNAs (piRNAs) that map to transposable elements (TEs) and 3'UTR of protein coding genes. Unusually, many TEs and the 3'UTR of some endogenous genes produce an abundant peak of 29-nt small RNAs with piRNA-like characteristics. Moreover, both sense and antisense piRNAs from TEs in both Anopheles gambiae and Drosophila melanogaster reveal novel features of piRNA sequence bias. We also discovered endogenous small interfering RNAs (endo-siRNAs) that map to overlapping transcripts and TEs. CONCLUSIONS: This is the first description of the germline miRNome in a mosquito species and should prove a valuable resource for understanding gene regulation that underlies gametogenesis and reproductive capacity. We also provide the first evidence of a piRNA pathway that is active against transposons in the germline and our findings suggest novel piRNA sequence bias. The contribution of small RNA pathways to germline TE regulation and genome defence in general is an important finding for approaches aimed at manipulating mosquito populations through the use of selfish genetic elements.

Journal Article Type Article
Acceptance Date Jan 19, 2015
Publication Date Feb 19, 2015
Publicly Available Date Mar 28, 2024
Journal BMC Genomics
Publisher Springer Verlag
Pages 100 - ?
DOI https://doi.org/10.1186/s12864-015-1257-2
Keywords Mosquito, miRNAs, Small RNAs, piRNAs, Gametogenesis, Malaria, Genome defence, Transposons, Germline
Publisher URL https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-015-1257-2
PMID 25766668

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