Whole-genome duplication and the functional diversification of teleost fish hemoglobins

Juan C. Opazo, G. Tyler Butts, Mariana F. Nery, Jay F. Storz, Federico G. Hoffmann

Research output: Contribution to journalArticle

45 Citations (Scopus)

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 O2 delivery in the face of changing metabolic demands and environmental O2 availability during different ontogenetic stages. During the course of development, regulatory changes in blood-O2 transport are mediated by the expression of multiple, functionally distinct hemoglobin (Hb) isoforms that meet the particular O2-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.

Original languageEnglish (US)
Pages (from-to)140-153
Number of pages14
JournalMolecular biology and evolution
Volume30
Issue number1
DOIs
StatePublished - Jan 1 2013

Fingerprint

hemoglobin
teleost
Globins
Fishes
Hemoglobins
genome
Genome
fish
Genes
gene
Multigene Family
multigene family
functional properties
Vertebrates
ancestry
genes
Oviparity
vertebrates
Genomic Segmental Duplications
Lepisosteidae

Keywords

  • convergent evolution
  • gene duplication
  • gene family evolution
  • genome duplication

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Cite this

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.

In: Molecular biology and evolution, Vol. 30, No. 1, 01.01.2013, p. 140-153.

Research output: Contribution to journalArticle

Opazo, Juan C. ; Butts, G. Tyler ; Nery, Mariana F. ; Storz, Jay F. ; Hoffmann, Federico G. / Whole-genome duplication and the functional diversification of teleost fish hemoglobins. In: Molecular biology and evolution. 2013 ; Vol. 30, No. 1. pp. 140-153.
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