Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs

Piwi-interacting small RNAs (piRNA) play a key role in controlling the activity of transposable elements (TEs) in the animal germline. In diverse arthropod species, including the pathogen vectors mosquitoes, the piRNA pathway is also active in nongonadal somatic tissues, where its targets and functi...

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Main Authors: Sergei Funikov, Alexander Rezvykh, Natalia Akulenko, Jiangtao Liang, Igor V. Sharakhov, Alla Kalmykova
Format: Article
Language:English
Published: Taylor & Francis Group 2025-02-01
Series:RNA Biology
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Online Access:https://www.tandfonline.com/doi/10.1080/15476286.2025.2463812
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author Sergei Funikov
Alexander Rezvykh
Natalia Akulenko
Jiangtao Liang
Igor V. Sharakhov
Alla Kalmykova
author_facet Sergei Funikov
Alexander Rezvykh
Natalia Akulenko
Jiangtao Liang
Igor V. Sharakhov
Alla Kalmykova
author_sort Sergei Funikov
collection DOAJ
description Piwi-interacting small RNAs (piRNA) play a key role in controlling the activity of transposable elements (TEs) in the animal germline. In diverse arthropod species, including the pathogen vectors mosquitoes, the piRNA pathway is also active in nongonadal somatic tissues, where its targets and functions are less clear. Here, we studied the features of small RNA production in head and thorax tissues of an uninfected laboratory strain of Anopheles coluzzii focusing on the 24-32-nt-long RNAs. Small RNAs derived from repetitive elements constitute a minor fraction while most small RNAs process from long noncoding RNAs (lncRNAs) and protein-coding gene mRNAs. The majority of small RNAs derived from repetitive elements and lncRNAs exhibited typical piRNAs features. By contrast, majority of protein-coding gene-derived 24-32 nt small RNAs lack the hallmarks of piRNAs and have signatures of nontemplated 3’ end tailing. Most of the atypical small RNAs exhibit female-biased expression and originate from mitochondrial and nuclear genes involved in energy metabolism. We also identified atypical genic small RNAs in Anopheles gambiae somatic tissues, which further validates the noncanonical mechanism of their production. We discuss a novel mechanism of small RNA production in mosquito somatic tissues and the possible functional significance of genic small RNAs.
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issn 1547-6286
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spelling doaj-art-b0c02cba85c74889a13c07e1cea4ddda2025-02-07T07:19:18ZengTaylor & Francis GroupRNA Biology1547-62861555-85842025-02-0110.1080/15476286.2025.2463812Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAsSergei Funikov0Alexander Rezvykh1Natalia Akulenko2Jiangtao Liang3Igor V. Sharakhov4Alla Kalmykova5Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, RussiaEngelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, RussiaInstitute of Molecular Genetics, Russian Academy of Sciences, Moscow, RussiaDepartment of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA, USADepartment of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA, USAKoltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, RussiaPiwi-interacting small RNAs (piRNA) play a key role in controlling the activity of transposable elements (TEs) in the animal germline. In diverse arthropod species, including the pathogen vectors mosquitoes, the piRNA pathway is also active in nongonadal somatic tissues, where its targets and functions are less clear. Here, we studied the features of small RNA production in head and thorax tissues of an uninfected laboratory strain of Anopheles coluzzii focusing on the 24-32-nt-long RNAs. Small RNAs derived from repetitive elements constitute a minor fraction while most small RNAs process from long noncoding RNAs (lncRNAs) and protein-coding gene mRNAs. The majority of small RNAs derived from repetitive elements and lncRNAs exhibited typical piRNAs features. By contrast, majority of protein-coding gene-derived 24-32 nt small RNAs lack the hallmarks of piRNAs and have signatures of nontemplated 3’ end tailing. Most of the atypical small RNAs exhibit female-biased expression and originate from mitochondrial and nuclear genes involved in energy metabolism. We also identified atypical genic small RNAs in Anopheles gambiae somatic tissues, which further validates the noncanonical mechanism of their production. We discuss a novel mechanism of small RNA production in mosquito somatic tissues and the possible functional significance of genic small RNAs.https://www.tandfonline.com/doi/10.1080/15476286.2025.2463812Anopheles coluzziiatypical small RNAssomatic piRNAtransposable elementsmitochondrial small RNAspiRNA processing
spellingShingle Sergei Funikov
Alexander Rezvykh
Natalia Akulenko
Jiangtao Liang
Igor V. Sharakhov
Alla Kalmykova
Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
RNA Biology
Anopheles coluzzii
atypical small RNAs
somatic piRNA
transposable elements
mitochondrial small RNAs
piRNA processing
title Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
title_full Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
title_fullStr Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
title_full_unstemmed Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
title_short Analysis of somatic piRNAs in the malaria mosquito Anopheles coluzzii reveals atypical classes of genic small RNAs
title_sort analysis of somatic pirnas in the malaria mosquito anopheles coluzzii reveals atypical classes of genic small rnas
topic Anopheles coluzzii
atypical small RNAs
somatic piRNA
transposable elements
mitochondrial small RNAs
piRNA processing
url https://www.tandfonline.com/doi/10.1080/15476286.2025.2463812
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