Network architecture of transcriptomic stress responses in zebrafish embryos.

Protein-protein interaction (PPI) network topology can contribute to explaining fundamental properties of genes, from expression levels to evolutionary constraints. Genes central to a network are more likely to be both conserved and highly expressed, whereas genes that are able to evolve in response...

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Main Authors: Kaylee Beine, Lauric Feugere, Alexander P Turner, Katharina C Wollenberg Valero
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1013164
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author Kaylee Beine
Lauric Feugere
Alexander P Turner
Katharina C Wollenberg Valero
author_facet Kaylee Beine
Lauric Feugere
Alexander P Turner
Katharina C Wollenberg Valero
author_sort Kaylee Beine
collection DOAJ
description Protein-protein interaction (PPI) network topology can contribute to explaining fundamental properties of genes, from expression levels to evolutionary constraints. Genes central to a network are more likely to be both conserved and highly expressed, whereas genes that are able to evolve in response to selective pressures but expressed at lower levels are located on the periphery of the network. The stress response is likewise thought to be conserved and its associated genes highly expressed, however, experimental evidence for these patterns is limited. Therefore, we examined here whether the transcriptomic response to two environmental stressors (heat, UV, and their combination) is related to PPI architecture in zebrafish (Danio rerio) embryos. We show that stress response genes are situated more centrally in the PPI network. The transcriptomic response to heat was located in both central and peripheral positions, whereas UV response transcripts occupied central to intermediate positions. Network position was further linked to the magnitude of fold changes of genes and number of their associated phenotype GO terms. Across treatments, differentially expressed genes in different parts of the network affected identical phenotypes. Our results indicate that the zebrafish stress response is considered conserved but also have stressor-specific aspects. These properties can aid in better understanding the organismal response to diverse and co-occurring stressors. Given the speed of contemporary changes in aquatic ecosystems, our approach can aid in identifying novel key regulators of the systemic response to specific stressors.
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spelling doaj-art-cac14aca5c3643ebafbd37e668e9e8f42025-08-20T02:22:06ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582025-06-01216e101316410.1371/journal.pcbi.1013164Network architecture of transcriptomic stress responses in zebrafish embryos.Kaylee BeineLauric FeugereAlexander P TurnerKatharina C Wollenberg ValeroProtein-protein interaction (PPI) network topology can contribute to explaining fundamental properties of genes, from expression levels to evolutionary constraints. Genes central to a network are more likely to be both conserved and highly expressed, whereas genes that are able to evolve in response to selective pressures but expressed at lower levels are located on the periphery of the network. The stress response is likewise thought to be conserved and its associated genes highly expressed, however, experimental evidence for these patterns is limited. Therefore, we examined here whether the transcriptomic response to two environmental stressors (heat, UV, and their combination) is related to PPI architecture in zebrafish (Danio rerio) embryos. We show that stress response genes are situated more centrally in the PPI network. The transcriptomic response to heat was located in both central and peripheral positions, whereas UV response transcripts occupied central to intermediate positions. Network position was further linked to the magnitude of fold changes of genes and number of their associated phenotype GO terms. Across treatments, differentially expressed genes in different parts of the network affected identical phenotypes. Our results indicate that the zebrafish stress response is considered conserved but also have stressor-specific aspects. These properties can aid in better understanding the organismal response to diverse and co-occurring stressors. Given the speed of contemporary changes in aquatic ecosystems, our approach can aid in identifying novel key regulators of the systemic response to specific stressors.https://doi.org/10.1371/journal.pcbi.1013164
spellingShingle Kaylee Beine
Lauric Feugere
Alexander P Turner
Katharina C Wollenberg Valero
Network architecture of transcriptomic stress responses in zebrafish embryos.
PLoS Computational Biology
title Network architecture of transcriptomic stress responses in zebrafish embryos.
title_full Network architecture of transcriptomic stress responses in zebrafish embryos.
title_fullStr Network architecture of transcriptomic stress responses in zebrafish embryos.
title_full_unstemmed Network architecture of transcriptomic stress responses in zebrafish embryos.
title_short Network architecture of transcriptomic stress responses in zebrafish embryos.
title_sort network architecture of transcriptomic stress responses in zebrafish embryos
url https://doi.org/10.1371/journal.pcbi.1013164
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AT lauricfeugere networkarchitectureoftranscriptomicstressresponsesinzebrafishembryos
AT alexanderpturner networkarchitectureoftranscriptomicstressresponsesinzebrafishembryos
AT katharinacwollenbergvalero networkarchitectureoftranscriptomicstressresponsesinzebrafishembryos