Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes
Abstract Background Antarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened for Hsf1 -binding...
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crspringernat:10.1186/s12862-019-1524-y 2023-05-15T14:11:42+02:00 Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes Bogan, Samuel N. Place, Sean P. National Science Foundation Council on Ocean Affairs Science and Technology, California State University 2019 http://dx.doi.org/10.1186/s12862-019-1524-y http://link.springer.com/content/pdf/10.1186/s12862-019-1524-y.pdf http://link.springer.com/article/10.1186/s12862-019-1524-y/fulltext.html en eng Springer Science and Business Media LLC http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ CC-BY BMC Evolutionary Biology volume 19, issue 1 ISSN 1471-2148 Ecology, Evolution, Behavior and Systematics journal-article 2019 crspringernat https://doi.org/10.1186/s12862-019-1524-y 2022-01-04T09:17:07Z Abstract Background Antarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened for Hsf1 -binding sites, as Hsf1 is a master transcription factor of the heat shock response, and highly-conserved non-coding elements within proximal promoters of chaperone genes across 10 Antarctic notothens, 2 subpolar notothens, and 17 perciform fishes. We employed phylogenetic models of molecular evolution to determine whether (i) changes in motifs associated with Hsf1 -binding and/or (ii) relaxed purifying selection or exaptation at ancestral cis- regulatory elements coincided with the evolution of chaperone frontloading in Antarctic notothens. Results Antarctic notothens exhibited significantly fewer Hsf1 -binding sites per bp at chaperone promoters than subpolar notothens and Serranoidei, the most closely-related suborder to Notothenioidei included in this study. 90% of chaperone promoters exhibited accelerated substitution rates among Antarctic notothens relative to other perciformes. The proportion of bases undergoing accelerated evolution (i) was significantly greater in Antarctic notothens than in subpolar notothens and Perciformes in 70% of chaperone genes and (ii) increased among bases that were more conserved among perciformes. Lastly, we detected evidence of relaxed purifying selection and exaptation acting on ancestrally conserved cis- regulatory elements in the Antarctic notothen lineage and its major branches. Conclusion A large degree of turnover has occurred in Notothenioidei at chaperone promoter regions that are conserved among perciform fishes following adaptation to the cooling of the Southern Ocean. Additionally, derived reductions in Hsf1 -binding site frequency suggest cis- regulatory modifications to the classical heat shock response. Of note, turnover events within chaperone promoters were less frequent in the ancestral node of Antarctic notothens relative to younger Antarctic lineages. This suggests that cis -regulatory divergence at chaperone promoters may be greater between Antarctic notothen lineages than between subpolar and Antarctic clades. These findings demonstrate that strong selective forces have acted upon cis -regulatory elements of chaperone genes among Antarctic notothens. Article in Journal/Newspaper Antarc* Antarctic Southern Ocean Springer Nature (via Crossref) Antarctic Southern Ocean The Antarctic BMC Evolutionary Biology 19 1 |
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Springer Nature (via Crossref) |
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crspringernat |
language |
English |
topic |
Ecology, Evolution, Behavior and Systematics |
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Ecology, Evolution, Behavior and Systematics Bogan, Samuel N. Place, Sean P. Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
topic_facet |
Ecology, Evolution, Behavior and Systematics |
description |
Abstract Background Antarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened for Hsf1 -binding sites, as Hsf1 is a master transcription factor of the heat shock response, and highly-conserved non-coding elements within proximal promoters of chaperone genes across 10 Antarctic notothens, 2 subpolar notothens, and 17 perciform fishes. We employed phylogenetic models of molecular evolution to determine whether (i) changes in motifs associated with Hsf1 -binding and/or (ii) relaxed purifying selection or exaptation at ancestral cis- regulatory elements coincided with the evolution of chaperone frontloading in Antarctic notothens. Results Antarctic notothens exhibited significantly fewer Hsf1 -binding sites per bp at chaperone promoters than subpolar notothens and Serranoidei, the most closely-related suborder to Notothenioidei included in this study. 90% of chaperone promoters exhibited accelerated substitution rates among Antarctic notothens relative to other perciformes. The proportion of bases undergoing accelerated evolution (i) was significantly greater in Antarctic notothens than in subpolar notothens and Perciformes in 70% of chaperone genes and (ii) increased among bases that were more conserved among perciformes. Lastly, we detected evidence of relaxed purifying selection and exaptation acting on ancestrally conserved cis- regulatory elements in the Antarctic notothen lineage and its major branches. Conclusion A large degree of turnover has occurred in Notothenioidei at chaperone promoter regions that are conserved among perciform fishes following adaptation to the cooling of the Southern Ocean. Additionally, derived reductions in Hsf1 -binding site frequency suggest cis- regulatory modifications to the classical heat shock response. Of note, turnover events within chaperone promoters were less frequent in the ancestral node of Antarctic notothens relative to younger Antarctic lineages. This suggests that cis -regulatory divergence at chaperone promoters may be greater between Antarctic notothen lineages than between subpolar and Antarctic clades. These findings demonstrate that strong selective forces have acted upon cis -regulatory elements of chaperone genes among Antarctic notothens. |
author2 |
National Science Foundation Council on Ocean Affairs Science and Technology, California State University |
format |
Article in Journal/Newspaper |
author |
Bogan, Samuel N. Place, Sean P. |
author_facet |
Bogan, Samuel N. Place, Sean P. |
author_sort |
Bogan, Samuel N. |
title |
Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
title_short |
Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
title_full |
Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
title_fullStr |
Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
title_full_unstemmed |
Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes |
title_sort |
accelerated evolution at chaperone promoters among antarctic notothenioid fishes |
publisher |
Springer Science and Business Media LLC |
publishDate |
2019 |
url |
http://dx.doi.org/10.1186/s12862-019-1524-y http://link.springer.com/content/pdf/10.1186/s12862-019-1524-y.pdf http://link.springer.com/article/10.1186/s12862-019-1524-y/fulltext.html |
geographic |
Antarctic Southern Ocean The Antarctic |
geographic_facet |
Antarctic Southern Ocean The Antarctic |
genre |
Antarc* Antarctic Southern Ocean |
genre_facet |
Antarc* Antarctic Southern Ocean |
op_source |
BMC Evolutionary Biology volume 19, issue 1 ISSN 1471-2148 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1186/s12862-019-1524-y |
container_title |
BMC Evolutionary Biology |
container_volume |
19 |
container_issue |
1 |
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1766283900086124544 |