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Stress-mediated convergence of splicing landscapes in male and female rock doves

BACKGROUND: The process of alternative splicing provides a unique mechanism by which eukaryotes are able to produce numerous protein products from the same gene. Heightened variability in the proteome has been thought to potentiate increased behavioral complexity and response flexibility to environm...

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Autores principales: Lang, Andrew S., Austin, Suzanne H., Harris, Rayna M., Calisi, Rebecca M., MacManes, Matthew D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7092514/
https://www.ncbi.nlm.nih.gov/pubmed/32293250
http://dx.doi.org/10.1186/s12864-020-6600-6
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author Lang, Andrew S.
Austin, Suzanne H.
Harris, Rayna M.
Calisi, Rebecca M.
MacManes, Matthew D.
author_facet Lang, Andrew S.
Austin, Suzanne H.
Harris, Rayna M.
Calisi, Rebecca M.
MacManes, Matthew D.
author_sort Lang, Andrew S.
collection PubMed
description BACKGROUND: The process of alternative splicing provides a unique mechanism by which eukaryotes are able to produce numerous protein products from the same gene. Heightened variability in the proteome has been thought to potentiate increased behavioral complexity and response flexibility to environmental stimuli, thus contributing to more refined traits on which natural and sexual selection can act. While it has been long known that various forms of environmental stress can negatively affect sexual behavior and reproduction, we know little of how stress can affect the alternative splicing associated with these events, and less still about how splicing may differ between sexes. Using the model of the rock dove (Columba livia), our team previously uncovered sexual dimorphism in the basal and stress-responsive gene transcription of a biological system necessary for facilitating sexual behavior and reproduction, the hypothalamic-pituitary-gonadal (HPG) axis. In this study, we delve further into understanding the mechanistic underpinnings of how changes in the environment can affect reproduction by testing the alternative splicing response of the HPG axis to an external stressor in both sexes. RESULTS: This study reveals dramatic baseline differences in HPG alternative splicing between males and females. However, after subjecting subjects to a restraint stress paradigm, we found a significant reduction in these differences between the sexes. In both stress and control treatments, we identified a higher incidence of splicing activity in the pituitary in both sexes as compared to other tissues. Of these splicing events, the core exon event is the most abundant form of splicing and more frequently occurs in the coding regions of the gene. Overall, we observed less splicing activity in the 3’UTR (untranslated region) end of transcripts than the 5’UTR or coding regions. CONCLUSIONS: Our results provide vital new insight into sex-specific aspects of the stress response on the HPG axis at an unprecedented proximate level. Males and females uniquely respond to stress, yet exhibit splicing patterns suggesting a convergent, optimal splicing landscape for stress response. This information has the potential to inform evolutionary theory as well as the development of highly-specific drug targets for stress-induced reproductive dysfunction.
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spelling pubmed-70925142020-03-24 Stress-mediated convergence of splicing landscapes in male and female rock doves Lang, Andrew S. Austin, Suzanne H. Harris, Rayna M. Calisi, Rebecca M. MacManes, Matthew D. BMC Genomics Research Article BACKGROUND: The process of alternative splicing provides a unique mechanism by which eukaryotes are able to produce numerous protein products from the same gene. Heightened variability in the proteome has been thought to potentiate increased behavioral complexity and response flexibility to environmental stimuli, thus contributing to more refined traits on which natural and sexual selection can act. While it has been long known that various forms of environmental stress can negatively affect sexual behavior and reproduction, we know little of how stress can affect the alternative splicing associated with these events, and less still about how splicing may differ between sexes. Using the model of the rock dove (Columba livia), our team previously uncovered sexual dimorphism in the basal and stress-responsive gene transcription of a biological system necessary for facilitating sexual behavior and reproduction, the hypothalamic-pituitary-gonadal (HPG) axis. In this study, we delve further into understanding the mechanistic underpinnings of how changes in the environment can affect reproduction by testing the alternative splicing response of the HPG axis to an external stressor in both sexes. RESULTS: This study reveals dramatic baseline differences in HPG alternative splicing between males and females. However, after subjecting subjects to a restraint stress paradigm, we found a significant reduction in these differences between the sexes. In both stress and control treatments, we identified a higher incidence of splicing activity in the pituitary in both sexes as compared to other tissues. Of these splicing events, the core exon event is the most abundant form of splicing and more frequently occurs in the coding regions of the gene. Overall, we observed less splicing activity in the 3’UTR (untranslated region) end of transcripts than the 5’UTR or coding regions. CONCLUSIONS: Our results provide vital new insight into sex-specific aspects of the stress response on the HPG axis at an unprecedented proximate level. Males and females uniquely respond to stress, yet exhibit splicing patterns suggesting a convergent, optimal splicing landscape for stress response. This information has the potential to inform evolutionary theory as well as the development of highly-specific drug targets for stress-induced reproductive dysfunction. BioMed Central 2020-03-23 /pmc/articles/PMC7092514/ /pubmed/32293250 http://dx.doi.org/10.1186/s12864-020-6600-6 Text en © The Author(s). 2020 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/. 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 in a credit line to the data.
spellingShingle Research Article
Lang, Andrew S.
Austin, Suzanne H.
Harris, Rayna M.
Calisi, Rebecca M.
MacManes, Matthew D.
Stress-mediated convergence of splicing landscapes in male and female rock doves
title Stress-mediated convergence of splicing landscapes in male and female rock doves
title_full Stress-mediated convergence of splicing landscapes in male and female rock doves
title_fullStr Stress-mediated convergence of splicing landscapes in male and female rock doves
title_full_unstemmed Stress-mediated convergence of splicing landscapes in male and female rock doves
title_short Stress-mediated convergence of splicing landscapes in male and female rock doves
title_sort stress-mediated convergence of splicing landscapes in male and female rock doves
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7092514/
https://www.ncbi.nlm.nih.gov/pubmed/32293250
http://dx.doi.org/10.1186/s12864-020-6600-6
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