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Whole-Genome Duplication and the Functional Diversification of Teleost Fish Hemoglobins

Opazo, Juan C., Butts, G. Tyler, Nery, Mariana F., Storz, Jay F., Hoffmann, Federico G.·2013·Molecular Biology and Evolution
DOI 10.1093/molbev/mss212PMC PMC3525417
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Abstract

Subsequent to the two rounds of whole-genome duplication that occurred in the common ancestor of vertebrates, a third genome duplication occurred in the stem lineage of teleost fishes. This teleost-specific genome duplication (TGD) is thought to have provided genetic raw materials for the physiological, morphological, and behavioral diversification of this highly speciose group. The extreme physiological versatility of teleost fish is manifest in their diversity of blood-gas transport traits, which reflects the myriad solutions that have evolved to maintain tissue O(2) delivery in the face of changing metabolic demands and environmental O(2) availability during different ontogenetic stages. During the course of development, regulatory changes in blood-O(2) transport are mediated by the expression of multiple, functionally distinct hemoglobin (Hb) isoforms that meet the particular O(2)-transport challenges encountered by the developing embryo or fetus (in viviparous or oviparous species) and in free-swimming larvae and adults. The main objective of the present study was to assess the relative contributions of whole-genome duplication, large-scale segmental duplication, and small-scale gene duplication in producing the extraordinary functional diversity of teleost Hbs. To accomplish this, we integrated phylogenetic reconstructions with analyses of conserved synteny to characterize the genomic organization and evolutionary history of the globin gene clusters of teleosts. These results were then integrated with available experimental data on functional properties and developmental patterns of stage-specific gene expression. Our results indicate that multiple α- and β-globin genes were present in the common ancestor of gars (order Lepisoteiformes) and teleosts. The comparative genomic analysis revealed that teleosts possess a dual set of TGD-derived globin gene clusters, each of which has undergone lineage-specific changes in gene content via repeated duplication and deletion events. Phylogenetic reconstructions revealed that paralogous genes convergently evolved similar functional properties in different teleost lineages. Consistent with other recent studies of globin gene family evolution in vertebrates, our results revealed evidence for repeated evolutionary transitions in the developmental regulation of Hb synthesis.

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Crossref · 10.1093/molbev/mss212

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Figures

Fig. 1. Unscaled depiction of the genomic organization of the MN and LA globin gene clusters from representative teleost fishes, with the human α-globin gene cluster provided as reference. To facilitate comparisons, all clusters are presented in the same orientation as the zebrafish. Genes in the forward orientation are shown on top of the chromosome, whereas genes in the reverse orientation are shown below.
Fig. 1. Unscaled depiction of the genomic organization of the MN and LA globin gene clusters from representative teleost fishes, with the human α-globin gene cluster provided as reference. To facilitate comparisons, all clusters are presented in the same orientation as the zebrafish. Genes in the forward orientation are shown on top of the chromosome, whereas genes in the reverse orientation are shown below.CC BY-NC · PubMed Central
Fig. 2. Genomic structure of the MN and LA globin gene clusters of teleost fish. To facilitate comparisons, all clusters are presented in the same orientation as the zebrafish. Genes in the forward orientation are shown on top of the chromosome, whereas genes in the reverse orientation are shown below. The green-spotted puffer globin genes are assumed to have the same stage-specific expression profiles as their orthologous counterparts in fugu. The Hbb pseudogene in the zebrafish MN cluster is not drawn to scale. Gene labels are color coded based on the timing of their expression. Genes marked with an asterisk were not included in the phylogenetic analyses.
Fig. 2. Genomic structure of the MN and LA globin gene clusters of teleost fish. To facilitate comparisons, all clusters are presented in the same orientation as the zebrafish. Genes in the forward orientation are shown on top of the chromosome, whereas genes in the reverse orientation are shown below. The green-spotted puffer globin genes are assumed to have the same stage-specific expression profiles as their orthologous counterparts in fugu. The Hbb pseudogene in the zebrafish MN cluster is not drawn to scale. Gene labels are color coded based on the timing of their expression. Genes marked with an asterisk were not included in the phylogenetic analyses.CC BY-NC · PubMed Central
Fig. 3. Maximum likelihood phylogram depicting relationships among the globin sequences of seven representative teleost fishes. Phylogenetic reconstructions were based on the coding sequences of α- and β-globin genes (panels A and B, respectively). Cartilaginous fish globins were used as outgroup sequences, and tetrapod sequences were included for comparative purposes. Values on the nodes denote bootstrap support values (above) and Bayesian posterior probabilities (below). Branches are color coded according to the location of the genes: MN-linked genes are shown in blue, LA-linked genes are shown in orange, and the gar genes are in green. Labels are color coded based on the timing of their expression. The substitution models selected are listed in supplementary table S3, Supplementary Material online.
Fig. 3. Maximum likelihood phylogram depicting relationships among the globin sequences of seven representative teleost fishes. Phylogenetic reconstructions were based on the coding sequences of α- and β-globin genes (panels A and B, respectively). Cartilaginous fish globins were used as outgroup sequences, and tetrapod sequences were included for comparative purposes. Values on the nodes denote bootstrap support values (above) and Bayesian posterior probabilities (below). Branches are color coded according to the location of the genes: MN-linked genes are shown in blue, LA-linked genes are shown in orange, and the gar genes are in green. Labels are color coded based on the timing of their expression. The substitution models selected are listed in supplementary table S3, Supplementary Material online.CC BY-NC · PubMed Central
Fig. 4. Evolutionary model describing the duplicative origins of the LA and MN globin gene clusters of teleost fish and the inferred globin gene repertoire in the common ancestor of teleosts and gar, a nonteleost ray finned fish. All clusters depicted are hypothetical with the exception of the gar cluster. The order of the α- and β-globin genes on the hypothetical clusters is arbitrary.
Fig. 4. Evolutionary model describing the duplicative origins of the LA and MN globin gene clusters of teleost fish and the inferred globin gene repertoire in the common ancestor of teleosts and gar, a nonteleost ray finned fish. All clusters depicted are hypothetical with the exception of the gar cluster. The order of the α- and β-globin genes on the hypothetical clusters is arbitrary.CC BY-NC · PubMed Central
Fig. 5. Dot plots of intrachromosomal sequence similarity in the MN globin gene clusters of medaka and stickleback. The fragment includes all genes in the clusters in addition to 5 kb of flanking sequence. The diagonal self-identity plot is shown in gray, as are the low-complexity areas in the medaka cluster. Note that the intragenomic dot plot for the stickleback gene cluster shows longer tracts of internal similarity off the self-identity diagonal relative to that for the medaka gene cluster, shown in black.
Fig. 5. Dot plots of intrachromosomal sequence similarity in the MN globin gene clusters of medaka and stickleback. The fragment includes all genes in the clusters in addition to 5 kb of flanking sequence. The diagonal self-identity plot is shown in gray, as are the low-complexity areas in the medaka cluster. Note that the intragenomic dot plot for the stickleback gene cluster shows longer tracts of internal similarity off the self-identity diagonal relative to that for the medaka gene cluster, shown in black.CC BY-NC · PubMed Central
Fig. 6. Maximum likelihood phylogram depicting relationships among the globin genes of the seven fish species for which full genome sequence data were available, plus sequences of functionally annotated globins from other teleost species. The phylogenetic reconstructions were based on the amino acid sequences of α- and β-globins (panels A and B, respectively). Cartilaginous fish globins were used as outgroup sequences, and tetrapod sequences were included for comparative purposes. Values on the nodes denote bootstrap support values (above) and Bayesian posterior probabilities (below). Genes are color coded according to their time of expression. Genes expressed at the embryonic/larval stages are shown in magenta, genes expressed at the juvenile and/or adult stages are shown light blue, and genes expressed across all ontogenetic stages are shown in dark blue. Genes with no record of expression and genes from nonactinopterygian vertebrates are shown in gray. The substitution models selected are listed on supplementary table S3, Supplementary Material online.
Fig. 6. Maximum likelihood phylogram depicting relationships among the globin genes of the seven fish species for which full genome sequence data were available, plus sequences of functionally annotated globins from other teleost species. The phylogenetic reconstructions were based on the amino acid sequences of α- and β-globins (panels A and B, respectively). Cartilaginous fish globins were used as outgroup sequences, and tetrapod sequences were included for comparative purposes. Values on the nodes denote bootstrap support values (above) and Bayesian posterior probabilities (below). Genes are color coded according to their time of expression. Genes expressed at the embryonic/larval stages are shown in magenta, genes expressed at the juvenile and/or adult stages are shown light blue, and genes expressed across all ontogenetic stages are shown in dark blue. Genes with no record of expression and genes from nonactinopterygian vertebrates are shown in gray. The substitution models selected are listed on supplementary table S3, Supplementary Material online.CC BY-NC · PubMed Central

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Research works printed but not linked: 5

  1. Goodman, 1987, Pattern and process in vertebrate phylogeny revealed by coevolution of molecules and phylogenies, 140
  2. Hardison, 2001, Organization, evolution, and regulation of the globin genes, 95
  3. Ingermann, 1997, Vertebrate hemoglobins., 357
  4. Weber, 1990, Functional significance and structural basis of multiple hemoglobins with special reference to ectothermic vertebrates, 58
  5. Wells, 2009, Blood-gas transport and hemoglobin function: adaptations for functional and environmental hypoxia, 255

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Metadata

Authors
Opazo, J. C., Butts, G. T., Nery, M. F., Storz, J. F., & Hoffmann, F. G.
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2012-10-16
Volume
30
Issue
1
Pages
140-153
ISSN
  • 1537-1719
  • 0737-4038
DOI
10.1093/molbev/mss212
PMC
PMC3525417
Cited by
98
References
113
Language
en

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CoChat. (2026). Citation check: Whole-Genome Duplication and the Functional Diversification of Teleost Fish Hemoglobins. https://app.cochat.ai/papers/10.1093/molbev/mss212
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Opazo, J. C., Butts, G. T., Nery, M. F., Storz, J. F., & Hoffmann, F. G. (2013). Whole-Genome Duplication and the Functional Diversification of Teleost Fish Hemoglobins. Molecular Biology and Evolution. https://doi.org/10.1093/molbev/mss212

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