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Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera

BACKGROUND: Polyandrous social insects such as the honey bee are prime candidates for parental manipulation of gene expression in offspring. Although there is good evidence for parent-of-origin effects in honey bees the epigenetic mechanisms that underlie these effects remain a mystery. Small RNA mo...

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Autores principales: Watson, Owen T., Buchmann, Gabriele, Young, Paul, Lo, Kitty, Remnant, Emily J., Yagound, Boris, Shambrook, Mitch, Hill, Andrew F., Oldroyd, Benjamin P., Ashe, Alyson
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978429/
https://www.ncbi.nlm.nih.gov/pubmed/35379185
http://dx.doi.org/10.1186/s12864-022-08478-9
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author Watson, Owen T.
Buchmann, Gabriele
Young, Paul
Lo, Kitty
Remnant, Emily J.
Yagound, Boris
Shambrook, Mitch
Hill, Andrew F.
Oldroyd, Benjamin P.
Ashe, Alyson
author_facet Watson, Owen T.
Buchmann, Gabriele
Young, Paul
Lo, Kitty
Remnant, Emily J.
Yagound, Boris
Shambrook, Mitch
Hill, Andrew F.
Oldroyd, Benjamin P.
Ashe, Alyson
author_sort Watson, Owen T.
collection PubMed
description BACKGROUND: Polyandrous social insects such as the honey bee are prime candidates for parental manipulation of gene expression in offspring. Although there is good evidence for parent-of-origin effects in honey bees the epigenetic mechanisms that underlie these effects remain a mystery. Small RNA molecules such as miRNAs, piRNAs and siRNAs play important roles in transgenerational epigenetic inheritance and in the regulation of gene expression during development. RESULTS: Here we present the first characterisation of small RNAs present in honey bee reproductive tissues: ovaries, spermatheca, semen, fertilised and unfertilised eggs, and testes. We show that semen contains fewer piRNAs relative to eggs and ovaries, and that piRNAs and miRNAs which map antisense to genes involved in DNA regulation and developmental processes are differentially expressed between tissues. tRNA fragments are highly abundant in semen and have a similar profile to those seen in the semen of other animals. Intriguingly we also find abundant piRNAs that target the sex determination locus, suggesting that piRNAs may play a role in honey bee sex determination. CONCLUSIONS: We conclude that small RNAs may play a fundamental role in honey bee gametogenesis and reproduction and provide a plausible mechanism for parent-of-origin effects on gene expression and reproductive physiology. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08478-9.
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spelling pubmed-89784292022-04-05 Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera Watson, Owen T. Buchmann, Gabriele Young, Paul Lo, Kitty Remnant, Emily J. Yagound, Boris Shambrook, Mitch Hill, Andrew F. Oldroyd, Benjamin P. Ashe, Alyson BMC Genomics Research BACKGROUND: Polyandrous social insects such as the honey bee are prime candidates for parental manipulation of gene expression in offspring. Although there is good evidence for parent-of-origin effects in honey bees the epigenetic mechanisms that underlie these effects remain a mystery. Small RNA molecules such as miRNAs, piRNAs and siRNAs play important roles in transgenerational epigenetic inheritance and in the regulation of gene expression during development. RESULTS: Here we present the first characterisation of small RNAs present in honey bee reproductive tissues: ovaries, spermatheca, semen, fertilised and unfertilised eggs, and testes. We show that semen contains fewer piRNAs relative to eggs and ovaries, and that piRNAs and miRNAs which map antisense to genes involved in DNA regulation and developmental processes are differentially expressed between tissues. tRNA fragments are highly abundant in semen and have a similar profile to those seen in the semen of other animals. Intriguingly we also find abundant piRNAs that target the sex determination locus, suggesting that piRNAs may play a role in honey bee sex determination. CONCLUSIONS: We conclude that small RNAs may play a fundamental role in honey bee gametogenesis and reproduction and provide a plausible mechanism for parent-of-origin effects on gene expression and reproductive physiology. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08478-9. BioMed Central 2022-04-04 /pmc/articles/PMC8978429/ /pubmed/35379185 http://dx.doi.org/10.1186/s12864-022-08478-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Watson, Owen T.
Buchmann, Gabriele
Young, Paul
Lo, Kitty
Remnant, Emily J.
Yagound, Boris
Shambrook, Mitch
Hill, Andrew F.
Oldroyd, Benjamin P.
Ashe, Alyson
Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title_full Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title_fullStr Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title_full_unstemmed Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title_short Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera
title_sort abundant small rnas in the reproductive tissues and eggs of the honey bee, apis mellifera
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978429/
https://www.ncbi.nlm.nih.gov/pubmed/35379185
http://dx.doi.org/10.1186/s12864-022-08478-9
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