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The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila

PIWI-interacting RNAs (piRNAs) are predominantly produced in animal gonads to suppress transposons during germline development. Our understanding about the piRNA biogenesis and function is predominantly from studies of the Drosophila female germline. piRNA pathway function in the male germline, howe...

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Autores principales: Quénerch'du, Emilie, Anand, Amit, Kai, Toshie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911912/
https://www.ncbi.nlm.nih.gov/pubmed/27208314
http://dx.doi.org/10.1261/rna.055996.116
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author Quénerch'du, Emilie
Anand, Amit
Kai, Toshie
author_facet Quénerch'du, Emilie
Anand, Amit
Kai, Toshie
author_sort Quénerch'du, Emilie
collection PubMed
description PIWI-interacting RNAs (piRNAs) are predominantly produced in animal gonads to suppress transposons during germline development. Our understanding about the piRNA biogenesis and function is predominantly from studies of the Drosophila female germline. piRNA pathway function in the male germline, however, remains poorly understood. To study overall and stage-specific features of piRNAs during spermatogenesis, we analyzed small RNAs extracted from entire wild-type testes and stage-specific arrest mutant testes enriched with spermatogonia or primary spermatocytes. We show that most active piRNA clusters in the female germline do not majorly contribute to piRNAs in testes, and abundance patterns of piRNAs mapping to different transposon families also differ between male and female germlines. piRNA production is regulated in a stage-specific manner during spermatogenesis. The piRNAs in spermatogonia-enriched testes are predominantly transposon-mapping piRNAs, and almost half of those exhibit a ping-pong signature. In contrast, the primary spermatocyte-enriched testes have a dramatically high amount of piRNAs targeting repeats like suppressor of stellate and AT-chX. The transposon-mapping piRNAs in the primary spermatocyte stages lacking Argonaute3 expression also show a ping-pong signature, albeit to a lesser extent. Consistently, argonaute3 mutant testes also retain ping-pong signature–bearing piRNAs, suggesting that a noncanonical ping-pong cycle might act during spermatogenesis. Our study shows stage-specific regulation of piRNA biogenesis during spermatogenesis: An active ping-pong cycle produces abundant transposon-mapping piRNAs in spermatogonia, while in primary spermatocytes, piRNAs act to suppress the repeats and transposons.
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spelling pubmed-49119122017-07-01 The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila Quénerch'du, Emilie Anand, Amit Kai, Toshie RNA Article PIWI-interacting RNAs (piRNAs) are predominantly produced in animal gonads to suppress transposons during germline development. Our understanding about the piRNA biogenesis and function is predominantly from studies of the Drosophila female germline. piRNA pathway function in the male germline, however, remains poorly understood. To study overall and stage-specific features of piRNAs during spermatogenesis, we analyzed small RNAs extracted from entire wild-type testes and stage-specific arrest mutant testes enriched with spermatogonia or primary spermatocytes. We show that most active piRNA clusters in the female germline do not majorly contribute to piRNAs in testes, and abundance patterns of piRNAs mapping to different transposon families also differ between male and female germlines. piRNA production is regulated in a stage-specific manner during spermatogenesis. The piRNAs in spermatogonia-enriched testes are predominantly transposon-mapping piRNAs, and almost half of those exhibit a ping-pong signature. In contrast, the primary spermatocyte-enriched testes have a dramatically high amount of piRNAs targeting repeats like suppressor of stellate and AT-chX. The transposon-mapping piRNAs in the primary spermatocyte stages lacking Argonaute3 expression also show a ping-pong signature, albeit to a lesser extent. Consistently, argonaute3 mutant testes also retain ping-pong signature–bearing piRNAs, suggesting that a noncanonical ping-pong cycle might act during spermatogenesis. Our study shows stage-specific regulation of piRNA biogenesis during spermatogenesis: An active ping-pong cycle produces abundant transposon-mapping piRNAs in spermatogonia, while in primary spermatocytes, piRNAs act to suppress the repeats and transposons. Cold Spring Harbor Laboratory Press 2016-07 /pmc/articles/PMC4911912/ /pubmed/27208314 http://dx.doi.org/10.1261/rna.055996.116 Text en © 2016 Quénerch'du et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by the RNA Society for the first 12 months after the full-issue publication date (see http://rnajournal.cshlp.org/site/misc/terms.xhtml). After 12 months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Article
Quénerch'du, Emilie
Anand, Amit
Kai, Toshie
The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title_full The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title_fullStr The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title_full_unstemmed The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title_short The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila
title_sort pirna pathway is developmentally regulated during spermatogenesis in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911912/
https://www.ncbi.nlm.nih.gov/pubmed/27208314
http://dx.doi.org/10.1261/rna.055996.116
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