Gene duplication, genome duplication, and the functional diversification of vertebrate globins

Jay F. Storz, Juan C. Opazo, Federico G. Hoffmann

Research output: Contribution to journalReview article

62 Citations (Scopus)

Abstract

The functional diversification of the vertebrate globin gene superfamily provides an especially vivid illustration of the role of gene duplication and whole-genome duplication in promoting evolutionary innovation. For example, key globin proteins that evolved specialized functions in various aspects of oxidative metabolism and oxygen signaling pathways (hemoglobin [Hb], myoglobin [Mb], and cytoglobin [Cygb]) trace their origins to two whole-genome duplication events in the stem lineage of vertebrates. The retention of the proto-Hb and Mb genes in the ancestor of jawed vertebrates permitted a physiological division of labor between the oxygen-carrier function of Hb and the oxygen-storage function of Mb. In the Hb gene lineage, a subsequent tandem gene duplication gave rise to the proto α- and β-globin genes, which permitted the formation of multimeric Hbs composed of unlike subunits (α2β2). The evolution of this heteromeric quaternary structure was central to the emergence of Hb as a specialized oxygen-transport protein because it provided a mechanism for cooperative oxygen-binding and allosteric regulatory control. Subsequent rounds of duplication and divergence have produced diverse repertoires of α- and β-like globin genes that are ontogenetically regulated such that functionally distinct Hb isoforms are expressed during different stages of prenatal development and postnatal life. In the ancestor of jawless fishes, the proto Mb and Hb genes appear to have been secondarily lost, and the Cygb homolog evolved a specialized respiratory function in blood-oxygen transport. Phylogenetic and comparative genomic analyses of the vertebrate globin gene superfamily have revealed numerous instances in which paralogous globins have convergently evolved similar expression patterns and/or similar functional specializations in different organismal lineages.

Original languageEnglish (US)
Pages (from-to)469-478
Number of pages10
JournalMolecular Phylogenetics and Evolution
Volume66
Issue number2
DOIs
StatePublished - Feb 1 2013

Fingerprint

Gene Duplication
Globins
gene duplication
Vertebrates
hemoglobin
vertebrate
Hemoglobins
genome
vertebrates
Genome
myoglobin
Myoglobin
Oxygen
gene
oxygen
Genes
genes
ancestry
prenatal development
aerobiosis

Keywords

  • Cytoglobin
  • Globin gene family
  • Hemoglobin
  • Myoglobin
  • Neuroglobin
  • Whole-genome duplication

ASJC Scopus subject areas

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

Cite this

Gene duplication, genome duplication, and the functional diversification of vertebrate globins. / Storz, Jay F.; Opazo, Juan C.; Hoffmann, Federico G.

In: Molecular Phylogenetics and Evolution, Vol. 66, No. 2, 01.02.2013, p. 469-478.

Research output: Contribution to journalReview article

@article{02baf3f1b5024820b1c8d921428958b4,
title = "Gene duplication, genome duplication, and the functional diversification of vertebrate globins",
abstract = "The functional diversification of the vertebrate globin gene superfamily provides an especially vivid illustration of the role of gene duplication and whole-genome duplication in promoting evolutionary innovation. For example, key globin proteins that evolved specialized functions in various aspects of oxidative metabolism and oxygen signaling pathways (hemoglobin [Hb], myoglobin [Mb], and cytoglobin [Cygb]) trace their origins to two whole-genome duplication events in the stem lineage of vertebrates. The retention of the proto-Hb and Mb genes in the ancestor of jawed vertebrates permitted a physiological division of labor between the oxygen-carrier function of Hb and the oxygen-storage function of Mb. In the Hb gene lineage, a subsequent tandem gene duplication gave rise to the proto α- and β-globin genes, which permitted the formation of multimeric Hbs composed of unlike subunits (α2β2). The evolution of this heteromeric quaternary structure was central to the emergence of Hb as a specialized oxygen-transport protein because it provided a mechanism for cooperative oxygen-binding and allosteric regulatory control. Subsequent rounds of duplication and divergence have produced diverse repertoires of α- and β-like globin genes that are ontogenetically regulated such that functionally distinct Hb isoforms are expressed during different stages of prenatal development and postnatal life. In the ancestor of jawless fishes, the proto Mb and Hb genes appear to have been secondarily lost, and the Cygb homolog evolved a specialized respiratory function in blood-oxygen transport. Phylogenetic and comparative genomic analyses of the vertebrate globin gene superfamily have revealed numerous instances in which paralogous globins have convergently evolved similar expression patterns and/or similar functional specializations in different organismal lineages.",
keywords = "Cytoglobin, Globin gene family, Hemoglobin, Myoglobin, Neuroglobin, Whole-genome duplication",
author = "Storz, {Jay F.} and Opazo, {Juan C.} and Hoffmann, {Federico G.}",
year = "2013",
month = "2",
day = "1",
doi = "10.1016/j.ympev.2012.07.013",
language = "English (US)",
volume = "66",
pages = "469--478",
journal = "Molecular Phylogenetics and Evolution",
issn = "1055-7903",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Gene duplication, genome duplication, and the functional diversification of vertebrate globins

AU - Storz, Jay F.

AU - Opazo, Juan C.

AU - Hoffmann, Federico G.

PY - 2013/2/1

Y1 - 2013/2/1

N2 - The functional diversification of the vertebrate globin gene superfamily provides an especially vivid illustration of the role of gene duplication and whole-genome duplication in promoting evolutionary innovation. For example, key globin proteins that evolved specialized functions in various aspects of oxidative metabolism and oxygen signaling pathways (hemoglobin [Hb], myoglobin [Mb], and cytoglobin [Cygb]) trace their origins to two whole-genome duplication events in the stem lineage of vertebrates. The retention of the proto-Hb and Mb genes in the ancestor of jawed vertebrates permitted a physiological division of labor between the oxygen-carrier function of Hb and the oxygen-storage function of Mb. In the Hb gene lineage, a subsequent tandem gene duplication gave rise to the proto α- and β-globin genes, which permitted the formation of multimeric Hbs composed of unlike subunits (α2β2). The evolution of this heteromeric quaternary structure was central to the emergence of Hb as a specialized oxygen-transport protein because it provided a mechanism for cooperative oxygen-binding and allosteric regulatory control. Subsequent rounds of duplication and divergence have produced diverse repertoires of α- and β-like globin genes that are ontogenetically regulated such that functionally distinct Hb isoforms are expressed during different stages of prenatal development and postnatal life. In the ancestor of jawless fishes, the proto Mb and Hb genes appear to have been secondarily lost, and the Cygb homolog evolved a specialized respiratory function in blood-oxygen transport. Phylogenetic and comparative genomic analyses of the vertebrate globin gene superfamily have revealed numerous instances in which paralogous globins have convergently evolved similar expression patterns and/or similar functional specializations in different organismal lineages.

AB - The functional diversification of the vertebrate globin gene superfamily provides an especially vivid illustration of the role of gene duplication and whole-genome duplication in promoting evolutionary innovation. For example, key globin proteins that evolved specialized functions in various aspects of oxidative metabolism and oxygen signaling pathways (hemoglobin [Hb], myoglobin [Mb], and cytoglobin [Cygb]) trace their origins to two whole-genome duplication events in the stem lineage of vertebrates. The retention of the proto-Hb and Mb genes in the ancestor of jawed vertebrates permitted a physiological division of labor between the oxygen-carrier function of Hb and the oxygen-storage function of Mb. In the Hb gene lineage, a subsequent tandem gene duplication gave rise to the proto α- and β-globin genes, which permitted the formation of multimeric Hbs composed of unlike subunits (α2β2). The evolution of this heteromeric quaternary structure was central to the emergence of Hb as a specialized oxygen-transport protein because it provided a mechanism for cooperative oxygen-binding and allosteric regulatory control. Subsequent rounds of duplication and divergence have produced diverse repertoires of α- and β-like globin genes that are ontogenetically regulated such that functionally distinct Hb isoforms are expressed during different stages of prenatal development and postnatal life. In the ancestor of jawless fishes, the proto Mb and Hb genes appear to have been secondarily lost, and the Cygb homolog evolved a specialized respiratory function in blood-oxygen transport. Phylogenetic and comparative genomic analyses of the vertebrate globin gene superfamily have revealed numerous instances in which paralogous globins have convergently evolved similar expression patterns and/or similar functional specializations in different organismal lineages.

KW - Cytoglobin

KW - Globin gene family

KW - Hemoglobin

KW - Myoglobin

KW - Neuroglobin

KW - Whole-genome duplication

UR - http://www.scopus.com/inward/record.url?scp=84873096226&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84873096226&partnerID=8YFLogxK

U2 - 10.1016/j.ympev.2012.07.013

DO - 10.1016/j.ympev.2012.07.013

M3 - Review article

C2 - 22846683

AN - SCOPUS:84873096226

VL - 66

SP - 469

EP - 478

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

SN - 1055-7903

IS - 2

ER -