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Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks

Animals exhibit dramatic immediate behavioral plasticity in response to social interactions, and brief social interactions can shape the future social landscape. However, the molecular mechanisms contributing to behavioral plasticity are unclear. Here, we show that the genome dynamically responds to...

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Autores principales: Bukhari, Syed Abbas, Saul, Michael C., Seward, Christopher H., Zhang, Huimin, Bensky, Miles, James, Noelle, Zhao, Sihai Dave, Chandrasekaran, Sriram, Stubbs, Lisa, Bell, Alison M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5509087/
https://www.ncbi.nlm.nih.gov/pubmed/28704398
http://dx.doi.org/10.1371/journal.pgen.1006840
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author Bukhari, Syed Abbas
Saul, Michael C.
Seward, Christopher H.
Zhang, Huimin
Bensky, Miles
James, Noelle
Zhao, Sihai Dave
Chandrasekaran, Sriram
Stubbs, Lisa
Bell, Alison M.
author_facet Bukhari, Syed Abbas
Saul, Michael C.
Seward, Christopher H.
Zhang, Huimin
Bensky, Miles
James, Noelle
Zhao, Sihai Dave
Chandrasekaran, Sriram
Stubbs, Lisa
Bell, Alison M.
author_sort Bukhari, Syed Abbas
collection PubMed
description Animals exhibit dramatic immediate behavioral plasticity in response to social interactions, and brief social interactions can shape the future social landscape. However, the molecular mechanisms contributing to behavioral plasticity are unclear. Here, we show that the genome dynamically responds to social interactions with multiple waves of transcription associated with distinct molecular functions in the brain of male threespined sticklebacks, a species famous for its behavioral repertoire and evolution. Some biological functions (e.g., hormone activity) peaked soon after a brief territorial challenge and then declined, while others (e.g., immune response) peaked hours afterwards. We identify transcription factors that are predicted to coordinate waves of transcription associated with different components of behavioral plasticity. Next, using H3K27Ac as a marker of chromatin accessibility, we show that a brief territorial intrusion was sufficient to cause rapid and dramatic changes in the epigenome. Finally, we integrate the time course brain gene expression data with a transcriptional regulatory network, and link gene expression to changes in chromatin accessibility. This study reveals rapid and dramatic epigenomic plasticity in response to a brief, highly consequential social interaction.
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spelling pubmed-55090872017-08-07 Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks Bukhari, Syed Abbas Saul, Michael C. Seward, Christopher H. Zhang, Huimin Bensky, Miles James, Noelle Zhao, Sihai Dave Chandrasekaran, Sriram Stubbs, Lisa Bell, Alison M. PLoS Genet Research Article Animals exhibit dramatic immediate behavioral plasticity in response to social interactions, and brief social interactions can shape the future social landscape. However, the molecular mechanisms contributing to behavioral plasticity are unclear. Here, we show that the genome dynamically responds to social interactions with multiple waves of transcription associated with distinct molecular functions in the brain of male threespined sticklebacks, a species famous for its behavioral repertoire and evolution. Some biological functions (e.g., hormone activity) peaked soon after a brief territorial challenge and then declined, while others (e.g., immune response) peaked hours afterwards. We identify transcription factors that are predicted to coordinate waves of transcription associated with different components of behavioral plasticity. Next, using H3K27Ac as a marker of chromatin accessibility, we show that a brief territorial intrusion was sufficient to cause rapid and dramatic changes in the epigenome. Finally, we integrate the time course brain gene expression data with a transcriptional regulatory network, and link gene expression to changes in chromatin accessibility. This study reveals rapid and dramatic epigenomic plasticity in response to a brief, highly consequential social interaction. Public Library of Science 2017-07-13 /pmc/articles/PMC5509087/ /pubmed/28704398 http://dx.doi.org/10.1371/journal.pgen.1006840 Text en © 2017 Bukhari et al 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 use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bukhari, Syed Abbas
Saul, Michael C.
Seward, Christopher H.
Zhang, Huimin
Bensky, Miles
James, Noelle
Zhao, Sihai Dave
Chandrasekaran, Sriram
Stubbs, Lisa
Bell, Alison M.
Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title_full Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title_fullStr Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title_full_unstemmed Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title_short Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
title_sort temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5509087/
https://www.ncbi.nlm.nih.gov/pubmed/28704398
http://dx.doi.org/10.1371/journal.pgen.1006840
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