Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters

<p>Abstract</p> <p>Background</p> <p>The vertebrate globin genes encoding the α- and β-subunits of the tetrameric hemoglobins are clustered at two unlinked loci. The highly conserved linear order of the genes flanking the hemoglobins provides a strong anchor for inferri...

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Main Authors: Jakobsen Kjetill S, Wilson Robert C, Nederbragt Alexander J, Wetten Ola F, Edvardsen Rolf B, Andersen Øivind
Format: Article
Language:English
Published: BMC 2010-10-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/10/315
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author Jakobsen Kjetill S
Wilson Robert C
Nederbragt Alexander J
Wetten Ola F
Edvardsen Rolf B
Andersen Øivind
author_facet Jakobsen Kjetill S
Wilson Robert C
Nederbragt Alexander J
Wetten Ola F
Edvardsen Rolf B
Andersen Øivind
author_sort Jakobsen Kjetill S
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The vertebrate globin genes encoding the α- and β-subunits of the tetrameric hemoglobins are clustered at two unlinked loci. The highly conserved linear order of the genes flanking the hemoglobins provides a strong anchor for inferring common ancestry of the globin clusters. In fish, the number of <it>α-β-</it>linked globin genes varies considerably between different sublineages and seems to be related to prevailing physico-chemical conditions. Draft sequences of the Atlantic cod genome enabled us to determine the genomic organization of the globin repertoire in this marine species that copes with fluctuating environments of the temperate and Arctic regions.</p> <p>Results</p> <p>The Atlantic cod genome was shown to contain 14 globin genes, including nine hemoglobin genes organized in two unlinked clusters designated <it>β5-α1-β1-α4 </it>and <it>β3-β4-α2-α3-β2</it>. The diverged cod hemoglobin genes displayed different expression levels in adult fish, and tetrameric hemoglobins with or without a Root effect were predicted. The novel finding of maternally inherited hemoglobin mRNAs is consistent with a potential role played by fish hemoglobins in the non-specific immune response. <it>In silico </it>analysis of the six teleost genomes available showed that the two <it>α-β </it>globin clusters are flanked by paralogs of five duplicated genes, in agreement with the proposed teleost-specific duplication of the ancestral vertebrate globin cluster. Screening the genome of extant urochordate and cephalochordate species for conserved globin-flanking genes revealed linkage of <it>RHBDF1, MPG </it>and <it>ARHGAP17 </it>to globin genes in the tunicate <it>Ciona intestinalis</it>, while these genes together with <it>LCMT </it>are closely positioned in amphioxus (<it>Branchiostoma floridae</it>), but seem to be unlinked to the multiple globin genes identified in this species.</p> <p>Conclusion</p> <p>The plasticity of Atlantic cod to variable environmental conditions probably involves the expression of multiple globins with potentially different properties. The interspecific difference in number of fish hemoglobin genes contrasts with the highly conserved synteny of the flanking genes. The proximity of globin-flanking genes in the tunicate and amphioxus genomes resembles the <it>RHBDF1-MPG-α-globin-ARHGAP17-LCMT </it>linked genes in man and chicken. We hypothesize that the fusion of the three chordate linkage groups 3, 15 and 17 more than 800 MYA led to the ancestral vertebrate globin cluster during a geological period of increased atmospheric oxygen content.</p>
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spelling doaj.art-f9ccd725c63f401e96eb360780345fe22022-12-21T16:42:58ZengBMCBMC Evolutionary Biology1471-21482010-10-0110131510.1186/1471-2148-10-315Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clustersJakobsen Kjetill SWilson Robert CNederbragt Alexander JWetten Ola FEdvardsen Rolf BAndersen Øivind<p>Abstract</p> <p>Background</p> <p>The vertebrate globin genes encoding the α- and β-subunits of the tetrameric hemoglobins are clustered at two unlinked loci. The highly conserved linear order of the genes flanking the hemoglobins provides a strong anchor for inferring common ancestry of the globin clusters. In fish, the number of <it>α-β-</it>linked globin genes varies considerably between different sublineages and seems to be related to prevailing physico-chemical conditions. Draft sequences of the Atlantic cod genome enabled us to determine the genomic organization of the globin repertoire in this marine species that copes with fluctuating environments of the temperate and Arctic regions.</p> <p>Results</p> <p>The Atlantic cod genome was shown to contain 14 globin genes, including nine hemoglobin genes organized in two unlinked clusters designated <it>β5-α1-β1-α4 </it>and <it>β3-β4-α2-α3-β2</it>. The diverged cod hemoglobin genes displayed different expression levels in adult fish, and tetrameric hemoglobins with or without a Root effect were predicted. The novel finding of maternally inherited hemoglobin mRNAs is consistent with a potential role played by fish hemoglobins in the non-specific immune response. <it>In silico </it>analysis of the six teleost genomes available showed that the two <it>α-β </it>globin clusters are flanked by paralogs of five duplicated genes, in agreement with the proposed teleost-specific duplication of the ancestral vertebrate globin cluster. Screening the genome of extant urochordate and cephalochordate species for conserved globin-flanking genes revealed linkage of <it>RHBDF1, MPG </it>and <it>ARHGAP17 </it>to globin genes in the tunicate <it>Ciona intestinalis</it>, while these genes together with <it>LCMT </it>are closely positioned in amphioxus (<it>Branchiostoma floridae</it>), but seem to be unlinked to the multiple globin genes identified in this species.</p> <p>Conclusion</p> <p>The plasticity of Atlantic cod to variable environmental conditions probably involves the expression of multiple globins with potentially different properties. The interspecific difference in number of fish hemoglobin genes contrasts with the highly conserved synteny of the flanking genes. The proximity of globin-flanking genes in the tunicate and amphioxus genomes resembles the <it>RHBDF1-MPG-α-globin-ARHGAP17-LCMT </it>linked genes in man and chicken. We hypothesize that the fusion of the three chordate linkage groups 3, 15 and 17 more than 800 MYA led to the ancestral vertebrate globin cluster during a geological period of increased atmospheric oxygen content.</p>http://www.biomedcentral.com/1471-2148/10/315
spellingShingle Jakobsen Kjetill S
Wilson Robert C
Nederbragt Alexander J
Wetten Ola F
Edvardsen Rolf B
Andersen Øivind
Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
BMC Evolutionary Biology
title Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
title_full Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
title_fullStr Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
title_full_unstemmed Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
title_short Genomic organization and gene expression of the multiple globins in Atlantic cod: conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters
title_sort genomic organization and gene expression of the multiple globins in atlantic cod conservation of globin flanking genes in chordates infers the origin of the vertebrate globin clusters
url http://www.biomedcentral.com/1471-2148/10/315
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