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Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development

BACKGROUND: The PIWI/piRNA pathway is a conserved machinery important for germ cell development and fertility. This piRNA-guided molecular machinery is best known for repressing derepressed transposable elements (TE) during epigenomic reprogramming. The extent to which piRNAs are involved in modulat...

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Autores principales: Chang, Kai-Wei, Tseng, Yen-Tzu, Chen, Yi-Chen, Yu, Chih-Yun, Liao, Hung-Fu, Chen, Yi-Chun, Tu, Yu-Fan Evan, Wu, Shinn-Chih, Liu, I-Hsuan, Pinskaya, Marina, Morillion, Antonin, Pain, Bertrand, Lin, Shau-Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984780/
https://www.ncbi.nlm.nih.gov/pubmed/29859049
http://dx.doi.org/10.1186/s12864-018-4820-9
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author Chang, Kai-Wei
Tseng, Yen-Tzu
Chen, Yi-Chen
Yu, Chih-Yun
Liao, Hung-Fu
Chen, Yi-Chun
Tu, Yu-Fan Evan
Wu, Shinn-Chih
Liu, I-Hsuan
Pinskaya, Marina
Morillion, Antonin
Pain, Bertrand
Lin, Shau-Ping
author_facet Chang, Kai-Wei
Tseng, Yen-Tzu
Chen, Yi-Chen
Yu, Chih-Yun
Liao, Hung-Fu
Chen, Yi-Chun
Tu, Yu-Fan Evan
Wu, Shinn-Chih
Liu, I-Hsuan
Pinskaya, Marina
Morillion, Antonin
Pain, Bertrand
Lin, Shau-Ping
author_sort Chang, Kai-Wei
collection PubMed
description BACKGROUND: The PIWI/piRNA pathway is a conserved machinery important for germ cell development and fertility. This piRNA-guided molecular machinery is best known for repressing derepressed transposable elements (TE) during epigenomic reprogramming. The extent to which piRNAs are involved in modulating transcripts beyond TEs still need to be clarified, and it may be a stage-dependent event. We chose chicken germline as a study model because of the significantly lower TE complexity in the chicken genome compared to mammalian species. RESULTS: We generated high-confidence piRNA candidates in various stages across chicken germline development by 3′-end-methylation-enriched small RNA sequencing and in-house bioinformatics analysis. We observed a significant developmental stage-dependent loss of TE association and a shifting of the ping-pong cycle signatures. Moreover, the stage-dependent reciprocal abundance of LINE retrotransposons, CR1-C, and its associated piRNAs implicated the developmental stage-dependent role of piRNA machinery. The stage dependency of piRNA expression and its potential functions can be better addressed by analyzing the piRNA precursors/clusters. Interestingly, the new piRNA clusters identified from embryonic chicken testes revealed evolutionary conservation between chickens and mammals, which was previously thought to not exist. CONCLUSIONS: In this report, we provided an original chicken RNA resource and proposed an analytical methodology that can be used to investigate stage-dependent changes in piRNA compositions and their potential roles in TE regulation and beyond, and also revealed possible conserved functions of piRNAs in developing germ cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4820-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-59847802018-06-07 Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development Chang, Kai-Wei Tseng, Yen-Tzu Chen, Yi-Chen Yu, Chih-Yun Liao, Hung-Fu Chen, Yi-Chun Tu, Yu-Fan Evan Wu, Shinn-Chih Liu, I-Hsuan Pinskaya, Marina Morillion, Antonin Pain, Bertrand Lin, Shau-Ping BMC Genomics Research Article BACKGROUND: The PIWI/piRNA pathway is a conserved machinery important for germ cell development and fertility. This piRNA-guided molecular machinery is best known for repressing derepressed transposable elements (TE) during epigenomic reprogramming. The extent to which piRNAs are involved in modulating transcripts beyond TEs still need to be clarified, and it may be a stage-dependent event. We chose chicken germline as a study model because of the significantly lower TE complexity in the chicken genome compared to mammalian species. RESULTS: We generated high-confidence piRNA candidates in various stages across chicken germline development by 3′-end-methylation-enriched small RNA sequencing and in-house bioinformatics analysis. We observed a significant developmental stage-dependent loss of TE association and a shifting of the ping-pong cycle signatures. Moreover, the stage-dependent reciprocal abundance of LINE retrotransposons, CR1-C, and its associated piRNAs implicated the developmental stage-dependent role of piRNA machinery. The stage dependency of piRNA expression and its potential functions can be better addressed by analyzing the piRNA precursors/clusters. Interestingly, the new piRNA clusters identified from embryonic chicken testes revealed evolutionary conservation between chickens and mammals, which was previously thought to not exist. CONCLUSIONS: In this report, we provided an original chicken RNA resource and proposed an analytical methodology that can be used to investigate stage-dependent changes in piRNA compositions and their potential roles in TE regulation and beyond, and also revealed possible conserved functions of piRNAs in developing germ cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4820-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-06-01 /pmc/articles/PMC5984780/ /pubmed/29859049 http://dx.doi.org/10.1186/s12864-018-4820-9 Text en © The Author(s). 2018 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.
spellingShingle Research Article
Chang, Kai-Wei
Tseng, Yen-Tzu
Chen, Yi-Chen
Yu, Chih-Yun
Liao, Hung-Fu
Chen, Yi-Chun
Tu, Yu-Fan Evan
Wu, Shinn-Chih
Liu, I-Hsuan
Pinskaya, Marina
Morillion, Antonin
Pain, Bertrand
Lin, Shau-Ping
Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title_full Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title_fullStr Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title_full_unstemmed Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title_short Stage-dependent piRNAs in chicken implicated roles in modulating male germ cell development
title_sort stage-dependent pirnas in chicken implicated roles in modulating male germ cell development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984780/
https://www.ncbi.nlm.nih.gov/pubmed/29859049
http://dx.doi.org/10.1186/s12864-018-4820-9
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