Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression

Juan C. Opazo, Federico G. Hoffmann, Chandrasekhar Natarajan, Christopher C. Witt, Michael Berenbrink, Jay F. Storz

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

The apparent stasis in the evolution of avian chromosomes suggests that birds may have experienced relatively low rates of gene gain and loss in multigene families. To investigate this possibility and to explore the phenotypic consequences of variation in gene copy number, we examined evolutionary changes in the families of genes that encode the α- and β-type subunits of hemoglobin (Hb), the tetrameric α2β2 protein responsible for blood-O2 transport. A comparative genomic analysis of 52 bird species revealed that the size and membership composition of the α- and β-globin gene families have remained remarkably constant during approximately 100 My of avian evolution. Most interspecific variation in gene content is attributable to multiple independent inactivations of the αD-globin gene, which encodes the α-chain subunit of a functionally distinct Hb isoform (HbD) that is expressed in both embryonic and definitive erythrocytes. Due to consistent differences in O2-binding properties between HbD and the major adult-expressed Hb isoform, HbA (which incorporates products of the αA-globin gene), recurrent losses of αD-globin contribute to among-species variation in blood-O2 affinity. Analysis of HbA/HbD expression levels in the red blood cells of 122 bird species revealed high variability among lineages and strong phylogenetic signal. In comparison with the homologous gene clusters in mammals, the low retention rate for lineage-specific gene duplicates in the avian globin gene clusters suggests that the developmental regulation of Hb synthesis in birds may be more highly conserved, with orthologous genes having similar stage-specific expression profiles and similar functional properties in disparate taxa.

Original languageEnglish (US)
Pages (from-to)871-887
Number of pages17
JournalMolecular biology and evolution
Volume32
Issue number4
DOIs
StatePublished - Apr 1 2015

Fingerprint

Globins
hemoglobin
turnover
Protein Isoforms
Hemoglobins
gene
Birds
Genes
Multigene Family
multigene family
genes
birds
Hemoglobin Subunits
erythrocytes
Erythrocytes
Duplicate Genes
blood
gene dosage
duplicate genes
Gene Dosage

Keywords

  • avian genomics
  • gene deletion
  • gene duplication
  • gene family evolution
  • hemoglobin
  • protein evolution

ASJC Scopus subject areas

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

Cite this

Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression. / Opazo, Juan C.; Hoffmann, Federico G.; Natarajan, Chandrasekhar; Witt, Christopher C.; Berenbrink, Michael; Storz, Jay F.

In: Molecular biology and evolution, Vol. 32, No. 4, 01.04.2015, p. 871-887.

Research output: Contribution to journalArticle

Opazo, Juan C. ; Hoffmann, Federico G. ; Natarajan, Chandrasekhar ; Witt, Christopher C. ; Berenbrink, Michael ; Storz, Jay F. / Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression. In: Molecular biology and evolution. 2015 ; Vol. 32, No. 4. pp. 871-887.
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