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Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)

Conflict between genes inherited from the mother (matrigenes) and the father (patrigenes) is predicted to arise during social interactions among offspring if these genes are not evenly distributed among offspring genotypes. This intragenomic conflict drives parent-specific transcription patterns in...

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Autores principales: Bresnahan, Sean T., Lee, Ellen, Clark, Lindsay, Ma, Rong, Rangel, Juliana, Grozinger, Christina M., Li-Byarlay, Hongmei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258952/
https://www.ncbi.nlm.nih.gov/pubmed/37308882
http://dx.doi.org/10.1186/s12864-023-09411-4
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author Bresnahan, Sean T.
Lee, Ellen
Clark, Lindsay
Ma, Rong
Rangel, Juliana
Grozinger, Christina M.
Li-Byarlay, Hongmei
author_facet Bresnahan, Sean T.
Lee, Ellen
Clark, Lindsay
Ma, Rong
Rangel, Juliana
Grozinger, Christina M.
Li-Byarlay, Hongmei
author_sort Bresnahan, Sean T.
collection PubMed
description Conflict between genes inherited from the mother (matrigenes) and the father (patrigenes) is predicted to arise during social interactions among offspring if these genes are not evenly distributed among offspring genotypes. This intragenomic conflict drives parent-specific transcription patterns in offspring resulting from parent-specific epigenetic modifications. Previous tests of the kinship theory of intragenomic conflict in honey bees (Apis mellifera) provided evidence in support of theoretical predictions for variation in worker reproduction, which is associated with extreme variation in morphology and behavior. However, more subtle behaviors – such as aggression – have not been extensively studied. Additionally, the canonical epigenetic mark (DNA methylation) associated with parent-specific transcription in plant and mammalian model species does not appear to play the same role as in honey bees, and thus the molecular mechanisms underlying intragenomic conflict in this species is an open area of investigation. Here, we examined the role of intragenomic conflict in shaping aggression in honey bee workers through a reciprocal cross design and Oxford Nanopore direct RNA sequencing. We attempted to probe the underlying regulatory basis of this conflict through analyses of parent-specific RNA m6A and alternative splicing patterns. We report evidence that intragenomic conflict occurs in the context of honey bee aggression, with increased paternal and maternal allele-biased transcription in aggressive compared to non-aggressive bees, and higher paternal allele-biased transcription overall. However, we found no evidence to suggest that RNA m6A or alternative splicing mediate intragenomic conflict in this species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09411-4.
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spelling pubmed-102589522023-06-13 Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera) Bresnahan, Sean T. Lee, Ellen Clark, Lindsay Ma, Rong Rangel, Juliana Grozinger, Christina M. Li-Byarlay, Hongmei BMC Genomics Research Conflict between genes inherited from the mother (matrigenes) and the father (patrigenes) is predicted to arise during social interactions among offspring if these genes are not evenly distributed among offspring genotypes. This intragenomic conflict drives parent-specific transcription patterns in offspring resulting from parent-specific epigenetic modifications. Previous tests of the kinship theory of intragenomic conflict in honey bees (Apis mellifera) provided evidence in support of theoretical predictions for variation in worker reproduction, which is associated with extreme variation in morphology and behavior. However, more subtle behaviors – such as aggression – have not been extensively studied. Additionally, the canonical epigenetic mark (DNA methylation) associated with parent-specific transcription in plant and mammalian model species does not appear to play the same role as in honey bees, and thus the molecular mechanisms underlying intragenomic conflict in this species is an open area of investigation. Here, we examined the role of intragenomic conflict in shaping aggression in honey bee workers through a reciprocal cross design and Oxford Nanopore direct RNA sequencing. We attempted to probe the underlying regulatory basis of this conflict through analyses of parent-specific RNA m6A and alternative splicing patterns. We report evidence that intragenomic conflict occurs in the context of honey bee aggression, with increased paternal and maternal allele-biased transcription in aggressive compared to non-aggressive bees, and higher paternal allele-biased transcription overall. However, we found no evidence to suggest that RNA m6A or alternative splicing mediate intragenomic conflict in this species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09411-4. BioMed Central 2023-06-12 /pmc/articles/PMC10258952/ /pubmed/37308882 http://dx.doi.org/10.1186/s12864-023-09411-4 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
Bresnahan, Sean T.
Lee, Ellen
Clark, Lindsay
Ma, Rong
Rangel, Juliana
Grozinger, Christina M.
Li-Byarlay, Hongmei
Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title_full Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title_fullStr Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title_full_unstemmed Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title_short Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)
title_sort examining parent-of-origin effects on transcription and rna methylation in mediating aggressive behavior in honey bees (apis mellifera)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258952/
https://www.ncbi.nlm.nih.gov/pubmed/37308882
http://dx.doi.org/10.1186/s12864-023-09411-4
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