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Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans

Piwi-interacting RNAs (piRNAs) and small interfering RNAs (siRNAs) are distinct classes of small RNAs required for proper germline development. To identify the roles of piRNAs and siRNAs in regulating gene expression in Caenorhabditis elegans, we subjected small RNAs and mRNAs from the gonads of piR...

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Autores principales: Reed, Kailee J, Svendsen, Joshua M, Brown, Kristen C, Montgomery, Brooke E, Marks, Taylor N, Vijayasarathy, Tarah, Parker, Dylan M, Nishimura, Erin Osborne, Updike, Dustin L, Montgomery, Taiowa A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7038979/
https://www.ncbi.nlm.nih.gov/pubmed/31872227
http://dx.doi.org/10.1093/nar/gkz1178
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author Reed, Kailee J
Svendsen, Joshua M
Brown, Kristen C
Montgomery, Brooke E
Marks, Taylor N
Vijayasarathy, Tarah
Parker, Dylan M
Nishimura, Erin Osborne
Updike, Dustin L
Montgomery, Taiowa A
author_facet Reed, Kailee J
Svendsen, Joshua M
Brown, Kristen C
Montgomery, Brooke E
Marks, Taylor N
Vijayasarathy, Tarah
Parker, Dylan M
Nishimura, Erin Osborne
Updike, Dustin L
Montgomery, Taiowa A
author_sort Reed, Kailee J
collection PubMed
description Piwi-interacting RNAs (piRNAs) and small interfering RNAs (siRNAs) are distinct classes of small RNAs required for proper germline development. To identify the roles of piRNAs and siRNAs in regulating gene expression in Caenorhabditis elegans, we subjected small RNAs and mRNAs from the gonads of piRNA and siRNA defective mutants to high-throughput sequencing. We show that piRNAs and an abundant class of siRNAs known as WAGO-class 22G-RNAs are required for proper expression of spermatogenic and oogenic genes. WAGO-class 22G-RNAs are also broadly required for transposon silencing, whereas piRNAs are largely dispensable. piRNAs, however, have a critical role in controlling histone gene expression. In the absence of piRNAs, histone mRNAs are misrouted into the nuclear RNAi pathway involving the Argonaute HRDE-1, concurrent with a reduction in the expression of many histone mRNAs. We also show that high-level gene expression in the germline is correlated with high level 22G-RNA production. However, most highly expressed genes produce 22G-RNAs through a distinct pathway that presumably involves the Argonaute CSR-1. In contrast, genes targeted by the WAGO branch of the 22G-RNA pathway are typically poorly expressed and respond unpredictably to loss of 22G-RNAs. Our results point to broad roles for piRNAs and siRNAs in controlling gene expression in the C. elegans germline.
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spelling pubmed-70389792020-03-02 Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans Reed, Kailee J Svendsen, Joshua M Brown, Kristen C Montgomery, Brooke E Marks, Taylor N Vijayasarathy, Tarah Parker, Dylan M Nishimura, Erin Osborne Updike, Dustin L Montgomery, Taiowa A Nucleic Acids Res Gene regulation, Chromatin and Epigenetics Piwi-interacting RNAs (piRNAs) and small interfering RNAs (siRNAs) are distinct classes of small RNAs required for proper germline development. To identify the roles of piRNAs and siRNAs in regulating gene expression in Caenorhabditis elegans, we subjected small RNAs and mRNAs from the gonads of piRNA and siRNA defective mutants to high-throughput sequencing. We show that piRNAs and an abundant class of siRNAs known as WAGO-class 22G-RNAs are required for proper expression of spermatogenic and oogenic genes. WAGO-class 22G-RNAs are also broadly required for transposon silencing, whereas piRNAs are largely dispensable. piRNAs, however, have a critical role in controlling histone gene expression. In the absence of piRNAs, histone mRNAs are misrouted into the nuclear RNAi pathway involving the Argonaute HRDE-1, concurrent with a reduction in the expression of many histone mRNAs. We also show that high-level gene expression in the germline is correlated with high level 22G-RNA production. However, most highly expressed genes produce 22G-RNAs through a distinct pathway that presumably involves the Argonaute CSR-1. In contrast, genes targeted by the WAGO branch of the 22G-RNA pathway are typically poorly expressed and respond unpredictably to loss of 22G-RNAs. Our results point to broad roles for piRNAs and siRNAs in controlling gene expression in the C. elegans germline. Oxford University Press 2020-02-28 2019-12-24 /pmc/articles/PMC7038979/ /pubmed/31872227 http://dx.doi.org/10.1093/nar/gkz1178 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Gene regulation, Chromatin and Epigenetics
Reed, Kailee J
Svendsen, Joshua M
Brown, Kristen C
Montgomery, Brooke E
Marks, Taylor N
Vijayasarathy, Tarah
Parker, Dylan M
Nishimura, Erin Osborne
Updike, Dustin L
Montgomery, Taiowa A
Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title_full Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title_fullStr Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title_full_unstemmed Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title_short Widespread roles for piRNAs and WAGO-class siRNAs in shaping the germline transcriptome of Caenorhabditis elegans
title_sort widespread roles for pirnas and wago-class sirnas in shaping the germline transcriptome of caenorhabditis elegans
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7038979/
https://www.ncbi.nlm.nih.gov/pubmed/31872227
http://dx.doi.org/10.1093/nar/gkz1178
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