Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)

As the Southern Ocean cooled to −1.8 °C over the past 40 My, the teleostean clade Notothenioidei diversified and, under reduced selection pressure for an oxygen-transporting apparatus, became less reliant on hemoglobin and red blood cells. At the extreme of this trend, the crown group of Antarctic i...

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Published in:Molecular Biology and Evolution
Main Authors: Lau, Yuk-Ting, Parker, Sandra K., Near, Thomas J., Detrich, H. William
Format: Text
Language:English
Published: Oxford University Press 2012
Subjects:
Online Access:http://mbe.oxfordjournals.org/cgi/content/short/29/3/1071
https://doi.org/10.1093/molbev/msr278
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spelling fthighwire:oai:open-archive.highwire.org:molbiolevol:29/3/1071 2023-05-15T13:38:13+02:00 Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae) Lau, Yuk-Ting Parker, Sandra K. Near, Thomas J. Detrich, H. William 2012-03-01 00:00:00.0 text/html http://mbe.oxfordjournals.org/cgi/content/short/29/3/1071 https://doi.org/10.1093/molbev/msr278 en eng Oxford University Press http://mbe.oxfordjournals.org/cgi/content/short/29/3/1071 http://dx.doi.org/10.1093/molbev/msr278 Copyright (C) 2012, Society for Molecular Biology and Evolution Research Articles TEXT 2012 fthighwire https://doi.org/10.1093/molbev/msr278 2012-03-03T13:34:47Z As the Southern Ocean cooled to −1.8 °C over the past 40 My, the teleostean clade Notothenioidei diversified and, under reduced selection pressure for an oxygen-transporting apparatus, became less reliant on hemoglobin and red blood cells. At the extreme of this trend, the crown group of Antarctic icefishes (Channichthyidae) lost both components of oxygen transport. Under the decreased selection scenario, we hypothesized that the Antarctic dragonfishes (Bathydraconidae, the red-blooded sister clade to the icefishes) evolved lower blood hemoglobin concentrations because their globin gene complexes (α- and β-globin gene pairs linked by a regulatory intergene) transcribe globin mRNAs less effectively than those of basal notothenioids (e.g., the Nototheniidae [notothens]). To test our hypothesis, we 1) sequenced the α/β-intergenes of the adult globin complexes of three notothen and eight dragonfish species and 2) measured globin transcript levels in representative species from each group. The typical nototheniid intergene was ∼3–4 kb in length. The bathydraconid intergenes resolved into three subclasses (long [3.8 kb], intermediate [3.0 kb], and short [1.5–2.3 kb]) that corresponded to the three subclades proposed for the taxon. Although they varied in length due to indels, the three notothen and eight dragonfish intergenes contained a conserved ∼90-nt element that we have previously shown to be required for globin gene transcription. Using the quantitative polymerase chain reaction, we found that globin mRNA levels in red cells from one notothen species and from one species of each dragonfish subclade were equivalent statistically. Thus, our results indicate that the bathydraconids have evolved adult globin loci whose regulatory intergenes tend to be shorter than those of the more basal nototheniids yet are equivalent in transcriptional efficacy. Their low blood hemoglobin concentrations are most likely due to reduction in hematocrit. Text Antarc* Antarctic Southern Ocean HighWire Press (Stanford University) Antarctic Southern Ocean The Antarctic Molecular Biology and Evolution 29 3 1071 1080
institution Open Polar
collection HighWire Press (Stanford University)
op_collection_id fthighwire
language English
topic Research Articles
spellingShingle Research Articles
Lau, Yuk-Ting
Parker, Sandra K.
Near, Thomas J.
Detrich, H. William
Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
topic_facet Research Articles
description As the Southern Ocean cooled to −1.8 °C over the past 40 My, the teleostean clade Notothenioidei diversified and, under reduced selection pressure for an oxygen-transporting apparatus, became less reliant on hemoglobin and red blood cells. At the extreme of this trend, the crown group of Antarctic icefishes (Channichthyidae) lost both components of oxygen transport. Under the decreased selection scenario, we hypothesized that the Antarctic dragonfishes (Bathydraconidae, the red-blooded sister clade to the icefishes) evolved lower blood hemoglobin concentrations because their globin gene complexes (α- and β-globin gene pairs linked by a regulatory intergene) transcribe globin mRNAs less effectively than those of basal notothenioids (e.g., the Nototheniidae [notothens]). To test our hypothesis, we 1) sequenced the α/β-intergenes of the adult globin complexes of three notothen and eight dragonfish species and 2) measured globin transcript levels in representative species from each group. The typical nototheniid intergene was ∼3–4 kb in length. The bathydraconid intergenes resolved into three subclasses (long [3.8 kb], intermediate [3.0 kb], and short [1.5–2.3 kb]) that corresponded to the three subclades proposed for the taxon. Although they varied in length due to indels, the three notothen and eight dragonfish intergenes contained a conserved ∼90-nt element that we have previously shown to be required for globin gene transcription. Using the quantitative polymerase chain reaction, we found that globin mRNA levels in red cells from one notothen species and from one species of each dragonfish subclade were equivalent statistically. Thus, our results indicate that the bathydraconids have evolved adult globin loci whose regulatory intergenes tend to be shorter than those of the more basal nototheniids yet are equivalent in transcriptional efficacy. Their low blood hemoglobin concentrations are most likely due to reduction in hematocrit.
format Text
author Lau, Yuk-Ting
Parker, Sandra K.
Near, Thomas J.
Detrich, H. William
author_facet Lau, Yuk-Ting
Parker, Sandra K.
Near, Thomas J.
Detrich, H. William
author_sort Lau, Yuk-Ting
title Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
title_short Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
title_full Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
title_fullStr Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
title_full_unstemmed Evolution and Function of the Globin Intergenic Regulatory Regions of the Antarctic Dragonfishes (Notothenioidei: Bathydraconidae)
title_sort evolution and function of the globin intergenic regulatory regions of the antarctic dragonfishes (notothenioidei: bathydraconidae)
publisher Oxford University Press
publishDate 2012
url http://mbe.oxfordjournals.org/cgi/content/short/29/3/1071
https://doi.org/10.1093/molbev/msr278
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_relation http://mbe.oxfordjournals.org/cgi/content/short/29/3/1071
http://dx.doi.org/10.1093/molbev/msr278
op_rights Copyright (C) 2012, Society for Molecular Biology and Evolution
op_doi https://doi.org/10.1093/molbev/msr278
container_title Molecular Biology and Evolution
container_volume 29
container_issue 3
container_start_page 1071
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