Evolution and expression of tissue globins in ray-finned fishes

Michael D. Gallagher, Daniel J. MacQueen

Research output: Contribution to journalArticle

2 Citations (Scopus)
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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 languageEnglish
Pages (from-to)32-47
Number of pages16
JournalGenome biology and evolution
Volume9
Issue number1
Early online date9 Nov 2016
DOIs
Publication statusPublished - 1 Jan 2017

Fingerprint

Skates (Fish)
Globins
myoglobin
Actinopterygii
teleost
fish
genome
Myoglobin
Osteoglossiformes
gene
duplicate genes
gene expression
breathing
branching
salmonid
Genome
vertebrates
genomics
oxygen
vertebrate

Keywords

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

Cite this

Evolution and expression of tissue globins in ray-finned fishes. / Gallagher, Michael D.; MacQueen, Daniel J.

In: Genome biology and evolution, Vol. 9, No. 1, 01.01.2017, p. 32-47.

Research output: Contribution to journalArticle

Gallagher, Michael D. ; MacQueen, Daniel J. / Evolution and expression of tissue globins in ray-finned fishes. In: Genome biology and evolution. 2017 ; Vol. 9, No. 1. pp. 32-47.
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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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