Stress-mediated convergence of splicing landscapes in male and female rock doves
Abstract 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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-03-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-020-6600-6 |
| _version_ | 1818610931152715776 |
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| author | Andrew S. Lang Suzanne H. Austin Rayna M. Harris Rebecca M. Calisi Matthew D. MacManes |
| author_facet | Andrew S. Lang Suzanne H. Austin Rayna M. Harris Rebecca M. Calisi Matthew D. MacManes |
| author_sort | Andrew S. Lang |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-16T15:22:16Z |
| format | Article |
| id | doaj.art-befd0db1006b4da0acbde6d3a6519a9e |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-16T15:22:16Z |
| publishDate | 2020-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-befd0db1006b4da0acbde6d3a6519a9e2022-12-21T22:26:36ZengBMCBMC Genomics1471-21642020-03-0121111810.1186/s12864-020-6600-6Stress-mediated convergence of splicing landscapes in male and female rock dovesAndrew S. Lang0Suzanne H. Austin1Rayna M. Harris2Rebecca M. Calisi3Matthew D. MacManes4Department of Molecular, Cellular, and Biomedical Sciences, University of New HampshireDepartment of Neurobiology, Physiology and Behavior, University of CaliforniaDepartment of Neurobiology, Physiology and Behavior, University of CaliforniaDepartment of Neurobiology, Physiology and Behavior, University of CaliforniaDepartment of Molecular, Cellular, and Biomedical Sciences, University of New HampshireAbstract 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.http://link.springer.com/article/10.1186/s12864-020-6600-6Alternative splicingRNA-seqStress responseReproductive AxisHPG AxisOrganismal response |
| spellingShingle | Andrew S. Lang Suzanne H. Austin Rayna M. Harris Rebecca M. Calisi Matthew D. MacManes Stress-mediated convergence of splicing landscapes in male and female rock doves BMC Genomics Alternative splicing RNA-seq Stress response Reproductive Axis HPG Axis Organismal response |
| 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 | Alternative splicing RNA-seq Stress response Reproductive Axis HPG Axis Organismal response |
| url | http://link.springer.com/article/10.1186/s12864-020-6600-6 |
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