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Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens

BACKGROUND: Aggression is an evolutionarily conserved behavior critical for animal survival. In the fish Betta splendens, across different stages of fighting interactions, fighting opponents suffer from various stressors, especially from the great demand for oxygen. Using RNA sequencing, we profiled...

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Autores principales: Trieu-Duc, Vu, Oshima, Kenshiro, Matsumura, Kenya, Iwasaki, Yuri, Chiu, Ming-Tzu, Nikaido, Masato, Okada, Norihiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9150285/
https://www.ncbi.nlm.nih.gov/pubmed/35637454
http://dx.doi.org/10.1186/s12864-022-08609-2
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author Trieu-Duc, Vu
Oshima, Kenshiro
Matsumura, Kenya
Iwasaki, Yuri
Chiu, Ming-Tzu
Nikaido, Masato
Okada, Norihiro
author_facet Trieu-Duc, Vu
Oshima, Kenshiro
Matsumura, Kenya
Iwasaki, Yuri
Chiu, Ming-Tzu
Nikaido, Masato
Okada, Norihiro
author_sort Trieu-Duc, Vu
collection PubMed
description BACKGROUND: Aggression is an evolutionarily conserved behavior critical for animal survival. In the fish Betta splendens, across different stages of fighting interactions, fighting opponents suffer from various stressors, especially from the great demand for oxygen. Using RNA sequencing, we profiled differential alternative splicing (DAS) events in the brains of fish collected before fighting, during fighting, and after fighting to study the involvement of alternative splicing (AS) in the response to stress during the fight. RESULTS: We found that fighting interactions induced the greatest increase in AS in the ‘during-fighting’ fish, followed by that of the ‘after-fighting’ fish. Intron retention (IR) was the most enriched type among all the basic AS events. DAS genes were mainly associated with synapse assembly, ion transport, and regulation of protein secretion. We further observed that IR events significantly differentiated between winners and losers for 19 genes, which were associated with messenger RNA biogenesis, DNA repair, and transcription machinery. These genes share many common features, including shorter intron length and higher GC content. CONCLUSIONS: This study is the first comprehensive view of AS induced by fighting interactions in a fish species across different stages of those interactions, especially with respect to IR events in winners and losers. Together, these findings facilitate future investigations into transcriptome complexity and AS regulation in response to stress under the context of aggression in vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08609-2.
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spelling pubmed-91502852022-05-31 Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens Trieu-Duc, Vu Oshima, Kenshiro Matsumura, Kenya Iwasaki, Yuri Chiu, Ming-Tzu Nikaido, Masato Okada, Norihiro BMC Genomics Research BACKGROUND: Aggression is an evolutionarily conserved behavior critical for animal survival. In the fish Betta splendens, across different stages of fighting interactions, fighting opponents suffer from various stressors, especially from the great demand for oxygen. Using RNA sequencing, we profiled differential alternative splicing (DAS) events in the brains of fish collected before fighting, during fighting, and after fighting to study the involvement of alternative splicing (AS) in the response to stress during the fight. RESULTS: We found that fighting interactions induced the greatest increase in AS in the ‘during-fighting’ fish, followed by that of the ‘after-fighting’ fish. Intron retention (IR) was the most enriched type among all the basic AS events. DAS genes were mainly associated with synapse assembly, ion transport, and regulation of protein secretion. We further observed that IR events significantly differentiated between winners and losers for 19 genes, which were associated with messenger RNA biogenesis, DNA repair, and transcription machinery. These genes share many common features, including shorter intron length and higher GC content. CONCLUSIONS: This study is the first comprehensive view of AS induced by fighting interactions in a fish species across different stages of those interactions, especially with respect to IR events in winners and losers. Together, these findings facilitate future investigations into transcriptome complexity and AS regulation in response to stress under the context of aggression in vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08609-2. BioMed Central 2022-05-30 /pmc/articles/PMC9150285/ /pubmed/35637454 http://dx.doi.org/10.1186/s12864-022-08609-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (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
Trieu-Duc, Vu
Oshima, Kenshiro
Matsumura, Kenya
Iwasaki, Yuri
Chiu, Ming-Tzu
Nikaido, Masato
Okada, Norihiro
Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title_full Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title_fullStr Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title_full_unstemmed Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title_short Alternative splicing plays key roles in response to stress across different stages of fighting in the fish Betta splendens
title_sort alternative splicing plays key roles in response to stress across different stages of fighting in the fish betta splendens
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9150285/
https://www.ncbi.nlm.nih.gov/pubmed/35637454
http://dx.doi.org/10.1186/s12864-022-08609-2
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