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Abundant expression of somatic transposon-derived piRNAs throughout Tribolium castaneum embryogenesis

Ninova, Maria and Griffiths-Jones, Sam and Ronshaugen, Matthew (2017) Abundant expression of somatic transposon-derived piRNAs throughout Tribolium castaneum embryogenesis. Genome Biology, 18 (1). Art. No. 184. ISSN 1474-760X. PMCID PMC5613491. https://resolver.caltech.edu/CaltechAUTHORS:20170926-131134220

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[img] PDF (Orientation of RepeatMasker annotations within piRNA clusters. Left: the strand-bias of the top 50 most piRNA-enriched clusters of the T. castaneum genome. Right: the number of regions identified as homologous to known TEs by RepeatMasker on the ...) - Supplemental Material
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[img] PDF (Small RNA size profile throughout the development of D. virilis. Abundance and composition of small RNA reads of different sizes (17–51 nt) in small RNA sequencing libraries from different developmental stages of D. virilis. Reads of each size were ...) - Supplemental Material
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[img] PDF (Developmental expression of Tc-Ago3 (top) and Tc-Piwi/Aub (bottom) transcripts. Barplots show the relative levels (FPKM) of the corresponding transcripts in RNA sequencing libraries from oocytes, 8–16, 16–24 and 24–48-h intervals. Histograms show the ...) - Supplemental Material
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Abstract

Background: Piwi-interacting RNAs (piRNAs) are a class of short (~26–31-nucleotide) non-protein-coding RNAs expressed in the metazoan germline. The piRNA pathway in arthropods is best understood in the ovary of Drosophila melanogaster, where it acts to silence active transposable elements (TEs). Maternal loading of piRNAs in oocytes is further required for the inheritance of piRNA-mediated transposon defence. However, our understanding of the diversity, evolution and function of the piRNA complement beyond drosophilids is limited. The red flour beetle, Tribolium castaneum, is an emerging model organism separated from Drosophila by ~ 350 million years of evolution that displays a number of features ancestral to arthropods, including short germ embryogenesis. Here, we characterize the maternally deposited and zygotically expressed small RNA and mRNA complements throughout T. castaneum embryogenesis. Results: We find that beetle oocytes and embryos of all stages are abundant in heterogeneous ~ 28-nucleotide RNAs. These small RNAs originate from discrete genomic loci enriched in TE sequences and display the molecular signatures of transposon-derived piRNAs. In addition to the maternally loaded primary piRNAs, Tribolium embryos produce secondary piRNAs by the cleavage of zygotically activated TE transcripts via the ping-pong mechanism. The two Tribolium piRNA pathway effector proteins, Tc-Piwi/Aub and Tc-Ago3, are also expressed throughout the soma of early embryos. Conclusions: Our results show that the piRNA pathway in Tribolium is not restricted to the germline, but also operates in the embryo and may act to antagonize zygotically activated transposons. Taken together, these data highlight a functional divergence of the piRNA pathway between insects.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1186/s13059-017-1304-1DOIArticle
https://genomebiology.biomedcentral.com/articles/10.1186/s13059-017-1304-1PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5613491PubMed CentralArticle
ORCID:
AuthorORCID
Ninova, Maria0000-0001-5051-5502
Ronshaugen, Matthew0000-0001-5326-5924
Additional Information:© 2017 The Author(s). This 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. Received: 15 November 2016; Accepted: 18 August 2017; Published: 26 September 2017. We thank Sue Brown, Mario Stanke and Gregor Bucher for providing the T. castaneum r4.0 genome assembly and protein-coding gene annotations, and the University of Manchester Genome Technologies Facility for assistance with RNA library preparation and sequencing. M.N. was supported by a Wellcome Trust PhD Studentship (093161/Z/10/Z). Availability of data and material: RNA-seq datasets supporting the conclusions of this article are available in the GEO database, GSE63770 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE63770). Authors’ contributions: MN, MR and SG-J conceived the study, designed the experiments and wrote the manuscript. MN performed all experiments and data analyses and drafted the manuscript. All authors read and approved the final manuscript. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. The authors declare that they have no competing interests.
Funders:
Funding AgencyGrant Number
Wellcome Trust093161/Z/10/Z
Subject Keywords:piRNA Short-germband development Maternal-zygotic transition Maternal transcripts Ping-pong pathway Transposons Tribolium castaneum
Issue or Number:1
PubMed Central ID:PMC5613491
Record Number:CaltechAUTHORS:20170926-131134220
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170926-131134220
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:81839
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:26 Sep 2017 20:32
Last Modified:03 Oct 2019 18:47

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