Evolution and expression of tissue globins in ray-finned fishes

Michael D. Gallagher; Daniel J. MacQueen

doi:10.1093/gbe/evw266

Evolution and expression of tissue globins in ray-finned fishes

Michael D. Gallagher, Daniel J. MacQueen

Research output: Contribution to journal › Article › peer-review

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Abstract

The globin gene family encodes oxygen-binding hemeproteins conserved across the major branches of multicellular life. The origins and evolutionary histories of complete globin repertoires have been established for many vertebrates, but there remain major knowledge gaps for ray-finned fish. Therefore, we used phylogenetic, comparative genomic and gene expression analyses to discover and characterize canonical “non-blood” globin family members (i.e., myoglobin, cytoglobin, neuroglobin, globin-X, and globin-Y) across multiple ray-finned fish lineages, revealing novel gene duplicates (paralogs) conserved from whole genome duplication (WGD) and small-scale duplication events. Our key findings were that: (1) globin-X paralogs in teleosts have been retained from the teleost-specific WGD, (2) functional paralogs of cytoglobin, neuroglobin, and globin-X, but not myoglobin, have been conserved from the salmonid-specific WGD, (3) triplicate lineage-specific myoglobin paralogs are conserved in arowanas (Osteoglossiformes), which arose by tandem duplication and diverged under positive selection, (4) globin-Y is retained in multiple early branching fish lineages that diverged before teleosts, and (5) marked variation in tissue-specific expression of globin gene repertoires exists across ray-finned fish evolution, including several previously uncharacterized sites of expression. In this respect, our data provide an interesting link between myoglobin expression and the evolution of air breathing in teleosts. Together, our findings demonstrate great-unrecognized diversity in the repertoire and expression of nonblood globins that has arisen during ray-finned fish evolution.

Original language	English
Pages (from-to)	32-47
Number of pages	16
Journal	Genome biology and evolution
Volume	9
Issue number	1
Early online date	9 Nov 2016
DOIs	https://doi.org/10.1093/gbe/evw266
Publication status	Published - 1 Jan 2017

Bibliographical note

We thank Professor Ian A. Johnston FRSE and Dr Daniel Garcia de la Serrana (School of Biology, University of St. Andrews) for providing tissues samples for African butterflyfish and spotted gar. We are grateful to Professor Peter W.H. Holland FRS (Department of Zoology, University of Oxford) for sharing sequence databases for Osteoglossiformes. We thank Professor Christopher J. Secombes (Institute of Biological and Environmental Sciences, University of Aberdeen) for gifting rainbow trout used in the study. Mr Ronald McKay contributed towards Pantodon molecular work during his undergraduate research. MDG is a PhD student funded by the BBSRC EASTBIO Doctoral Training Partnership (DTP) (BB/J01446X/1). The study received support from institutional funds within the University of Aberdeen and from an undergraduate Research Experience Placement scheme granted by the BBSRC EASTBIO DTP scheme.

Keywords

oxygen transport
ray-finned fish
globin gene family
phylogeny
evolution
gene expression

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10.1093/gbe/evw266Licence: CC BY

Evolution and expression of tissue globins in ray-finned fishes
© The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Final published version, 2.1 MBLicence: CC BY

Cite this

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abstract = "The globin gene family encodes oxygen-binding hemeproteins conserved across the major branches of multicellular life. The origins and evolutionary histories of complete globin repertoires have been established for many vertebrates, but there remain major knowledge gaps for ray-finned fish. Therefore, we used phylogenetic, comparative genomic and gene expression analyses to discover and characterize canonical “non-blood” globin family members (i.e., myoglobin, cytoglobin, neuroglobin, globin-X, and globin-Y) across multiple ray-finned fish lineages, revealing novel gene duplicates (paralogs) conserved from whole genome duplication (WGD) and small-scale duplication events. Our key findings were that: (1) globin-X paralogs in teleosts have been retained from the teleost-specific WGD, (2) functional paralogs of cytoglobin, neuroglobin, and globin-X, but not myoglobin, have been conserved from the salmonid-specific WGD, (3) triplicate lineage-specific myoglobin paralogs are conserved in arowanas (Osteoglossiformes), which arose by tandem duplication and diverged under positive selection, (4) globin-Y is retained in multiple early branching fish lineages that diverged before teleosts, and (5) marked variation in tissue-specific expression of globin gene repertoires exists across ray-finned fish evolution, including several previously uncharacterized sites of expression. In this respect, our data provide an interesting link between myoglobin expression and the evolution of air breathing in teleosts. Together, our findings demonstrate great-unrecognized diversity in the repertoire and expression of nonblood globins that has arisen during ray-finned fish evolution.",

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note = "We thank Professor Ian A. Johnston FRSE and Dr Daniel Garcia de la Serrana (School of Biology, University of St. Andrews) for providing tissues samples for African butterflyfish and spotted gar. We are grateful to Professor Peter W.H. Holland FRS (Department of Zoology, University of Oxford) for sharing sequence databases for Osteoglossiformes. We thank Professor Christopher J. Secombes (Institute of Biological and Environmental Sciences, University of Aberdeen) for gifting rainbow trout used in the study. Mr Ronald McKay contributed towards Pantodon molecular work during his undergraduate research. MDG is a PhD student funded by the BBSRC EASTBIO Doctoral Training Partnership (DTP) (BB/J01446X/1). The study received support from institutional funds within the University of Aberdeen and from an undergraduate Research Experience Placement scheme granted by the BBSRC EASTBIO DTP scheme.",

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AU - MacQueen, Daniel J.

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N2 - The globin gene family encodes oxygen-binding hemeproteins conserved across the major branches of multicellular life. The origins and evolutionary histories of complete globin repertoires have been established for many vertebrates, but there remain major knowledge gaps for ray-finned fish. Therefore, we used phylogenetic, comparative genomic and gene expression analyses to discover and characterize canonical “non-blood” globin family members (i.e., myoglobin, cytoglobin, neuroglobin, globin-X, and globin-Y) across multiple ray-finned fish lineages, revealing novel gene duplicates (paralogs) conserved from whole genome duplication (WGD) and small-scale duplication events. Our key findings were that: (1) globin-X paralogs in teleosts have been retained from the teleost-specific WGD, (2) functional paralogs of cytoglobin, neuroglobin, and globin-X, but not myoglobin, have been conserved from the salmonid-specific WGD, (3) triplicate lineage-specific myoglobin paralogs are conserved in arowanas (Osteoglossiformes), which arose by tandem duplication and diverged under positive selection, (4) globin-Y is retained in multiple early branching fish lineages that diverged before teleosts, and (5) marked variation in tissue-specific expression of globin gene repertoires exists across ray-finned fish evolution, including several previously uncharacterized sites of expression. In this respect, our data provide an interesting link between myoglobin expression and the evolution of air breathing in teleosts. Together, our findings demonstrate great-unrecognized diversity in the repertoire and expression of nonblood globins that has arisen during ray-finned fish evolution.

AB - The globin gene family encodes oxygen-binding hemeproteins conserved across the major branches of multicellular life. The origins and evolutionary histories of complete globin repertoires have been established for many vertebrates, but there remain major knowledge gaps for ray-finned fish. Therefore, we used phylogenetic, comparative genomic and gene expression analyses to discover and characterize canonical “non-blood” globin family members (i.e., myoglobin, cytoglobin, neuroglobin, globin-X, and globin-Y) across multiple ray-finned fish lineages, revealing novel gene duplicates (paralogs) conserved from whole genome duplication (WGD) and small-scale duplication events. Our key findings were that: (1) globin-X paralogs in teleosts have been retained from the teleost-specific WGD, (2) functional paralogs of cytoglobin, neuroglobin, and globin-X, but not myoglobin, have been conserved from the salmonid-specific WGD, (3) triplicate lineage-specific myoglobin paralogs are conserved in arowanas (Osteoglossiformes), which arose by tandem duplication and diverged under positive selection, (4) globin-Y is retained in multiple early branching fish lineages that diverged before teleosts, and (5) marked variation in tissue-specific expression of globin gene repertoires exists across ray-finned fish evolution, including several previously uncharacterized sites of expression. In this respect, our data provide an interesting link between myoglobin expression and the evolution of air breathing in teleosts. Together, our findings demonstrate great-unrecognized diversity in the repertoire and expression of nonblood globins that has arisen during ray-finned fish evolution.

KW - oxygen transport

KW - ray-finned fish

KW - globin gene family

KW - phylogeny

KW - evolution

KW - gene expression

U2 - 10.1093/gbe/evw266

DO - 10.1093/gbe/evw266

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EP - 47

JO - Genome biology and evolution

JF - Genome biology and evolution

IS - 1

ER -

Evolution and expression of tissue globins in ray-finned fishes

Abstract

Bibliographical note

Keywords

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