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The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus

BACKGROUND: The function of DNA methyltransferase genes of insects is a puzzle, because an association between gene expression and methylation is not universal for insects. If the genes normally involved in cytosine methylation are not influencing gene expression, what might be their role? We previo...

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Autores principales: Cunningham, Christopher B., Shelby, Emily A., McKinney, Elizabeth C., Schmitz, Robert J., Moore, Allen J., Moore, Patricia J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10314392/
https://www.ncbi.nlm.nih.gov/pubmed/37393253
http://dx.doi.org/10.1186/s13072-023-00496-5
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author Cunningham, Christopher B.
Shelby, Emily A.
McKinney, Elizabeth C.
Schmitz, Robert J.
Moore, Allen J.
Moore, Patricia J.
author_facet Cunningham, Christopher B.
Shelby, Emily A.
McKinney, Elizabeth C.
Schmitz, Robert J.
Moore, Allen J.
Moore, Patricia J.
author_sort Cunningham, Christopher B.
collection PubMed
description BACKGROUND: The function of DNA methyltransferase genes of insects is a puzzle, because an association between gene expression and methylation is not universal for insects. If the genes normally involved in cytosine methylation are not influencing gene expression, what might be their role? We previously demonstrated that gametogenesis of Oncopeltus fasciatus is interrupted at meiosis following knockdown of DNA methyltransferase 1 (Dnmt1) and this is unrelated to changes in levels of cytosine methylation. Here, using transcriptomics, we tested the hypothesis that Dmnt1 is a part of the meiotic gene pathway. Testes, which almost exclusively contain gametes at varying stages of development, were sampled at 7 days and 14 days following knockdown of Dmnt1 using RNAi. RESULTS: Using microscopy, we found actively dividing spermatocysts were reduced at both timepoints. However, as with other studies, we saw Dnmt1 knockdown resulted in condensed nuclei after mitosis–meiosis transition, and then cellular arrest. We found limited support for a functional role for Dnmt1 in our predicted cell cycle and meiotic pathways. An examination of a priori Gene Ontology terms showed no enrichment for meiosis. We then used the full data set to reveal further candidate pathways influenced by Dnmt1 for further hypotheses. Very few genes were differentially expressed at 7 days, but nearly half of all transcribed genes were differentially expressed at 14 days. We found no strong candidate pathways for how Dnmt1 knockdown was achieving its effect through Gene Ontology term overrepresentation analysis. CONCLUSIONS: We, therefore, suggest that Dmnt1 plays a role in chromosome dynamics based on our observations of condensed nuclei and cellular arrest with no specific molecular pathways disrupted. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13072-023-00496-5.
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spelling pubmed-103143922023-07-02 The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus Cunningham, Christopher B. Shelby, Emily A. McKinney, Elizabeth C. Schmitz, Robert J. Moore, Allen J. Moore, Patricia J. Epigenetics Chromatin Research BACKGROUND: The function of DNA methyltransferase genes of insects is a puzzle, because an association between gene expression and methylation is not universal for insects. If the genes normally involved in cytosine methylation are not influencing gene expression, what might be their role? We previously demonstrated that gametogenesis of Oncopeltus fasciatus is interrupted at meiosis following knockdown of DNA methyltransferase 1 (Dnmt1) and this is unrelated to changes in levels of cytosine methylation. Here, using transcriptomics, we tested the hypothesis that Dmnt1 is a part of the meiotic gene pathway. Testes, which almost exclusively contain gametes at varying stages of development, were sampled at 7 days and 14 days following knockdown of Dmnt1 using RNAi. RESULTS: Using microscopy, we found actively dividing spermatocysts were reduced at both timepoints. However, as with other studies, we saw Dnmt1 knockdown resulted in condensed nuclei after mitosis–meiosis transition, and then cellular arrest. We found limited support for a functional role for Dnmt1 in our predicted cell cycle and meiotic pathways. An examination of a priori Gene Ontology terms showed no enrichment for meiosis. We then used the full data set to reveal further candidate pathways influenced by Dnmt1 for further hypotheses. Very few genes were differentially expressed at 7 days, but nearly half of all transcribed genes were differentially expressed at 14 days. We found no strong candidate pathways for how Dnmt1 knockdown was achieving its effect through Gene Ontology term overrepresentation analysis. CONCLUSIONS: We, therefore, suggest that Dmnt1 plays a role in chromosome dynamics based on our observations of condensed nuclei and cellular arrest with no specific molecular pathways disrupted. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13072-023-00496-5. BioMed Central 2023-07-01 /pmc/articles/PMC10314392/ /pubmed/37393253 http://dx.doi.org/10.1186/s13072-023-00496-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Cunningham, Christopher B.
Shelby, Emily A.
McKinney, Elizabeth C.
Schmitz, Robert J.
Moore, Allen J.
Moore, Patricia J.
The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title_full The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title_fullStr The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title_full_unstemmed The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title_short The role of Dmnt1 during spermatogenesis of the insect Oncopeltus fasciatus
title_sort role of dmnt1 during spermatogenesis of the insect oncopeltus fasciatus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10314392/
https://www.ncbi.nlm.nih.gov/pubmed/37393253
http://dx.doi.org/10.1186/s13072-023-00496-5
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