Lineage-specific patterns of functional diversification in the α-and β-globin gene families of tetrapod vertebrates

Federico G. Hoffmann, Jay F. Storz, Thomas A. Gorr, Juan C. Opazo

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

The α-and β-globin gene families of jawed vertebrates have diversified with respect to both gene function and the developmental timing of gene expression. Phylogenetic reconstructions of globin gene family evolution have provided suggestive evidence that the developmental regulation of hemoglobin synthesis has evolved independently in multiple vertebrate lineages. For example, the embryonic β-like globin genes of birds and placental mammals are not 1:1 orthologs. Despite the similarity in developmental expression profiles, the genes are independently derived from lineage-specific duplications of a β-globin pro-ortholog. This suggests the possibility that other vertebrate taxa may also possess distinct repertoires of globin genes that were produced by repeated rounds of lineage-specific gene duplication and divergence. Until recently, investigations into this possibility have been hindered by the dearth of genomic sequence data from nonmammalian vertebrates. Here, we report new insights into globin gene family evolution that were provided by a phylogenetic analysis of vertebrate globins combined with a comparative genomic analysis of three key sauropsid taxa: a squamate reptile (anole lizard, Anolis carolinensis), a passeriform bird (zebra finch, Taeniopygia guttata), and a galliform bird (chicken, Gallus gallus). The main objectives of this study were 1) to characterize evolutionary changes in the size and membership composition of the α-and β-globin gene families of tetrapod vertebrates and 2) to test whether functional diversification of the globin gene clusters occurred independently in different tetrapod lineages. Results of our comparative genomic analysis revealed several intriguing patterns of gene turnover in the globin gene clusters of different taxa. Lineage-specific differences in gene content were especially pronounced in the β-globin gene family, as phylogenetic reconstructions revealed that amphibians, lepidosaurs (as represented by anole lizard), archosaurs (as represented by zebra finch and chicken), and mammals each possess a distinct independently derived repertoire of β-like globin genes. In contrast to the ancient functional diversification of the α-globin gene cluster in the stem lineage of tetrapods, the physiological division of labor between early-and late-expressed genes in the β-globin gene cluster appears to have evolved independently in several tetrapod lineages.

Original languageEnglish (US)
Pages (from-to)1126-1138
Number of pages13
JournalMolecular biology and evolution
Volume27
Issue number5
DOIs
StatePublished - May 2010

Fingerprint

Globins
tetrapod
Vertebrates
vertebrate
vertebrates
gene
Genes
genes
multigene family
Multigene Family
Taeniopygia guttata
Birds
Finches
Chickens
Lizards
Equidae
genomics
family
lizards
birds

Keywords

  • Anolis
  • Gene duplication
  • Gene family evolution
  • Genome evolution
  • Hemoglobin
  • Zebra finch

ASJC Scopus subject areas

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

Cite this

Lineage-specific patterns of functional diversification in the α-and β-globin gene families of tetrapod vertebrates. / Hoffmann, Federico G.; Storz, Jay F.; Gorr, Thomas A.; Opazo, Juan C.

In: Molecular biology and evolution, Vol. 27, No. 5, 05.2010, p. 1126-1138.

Research output: Contribution to journalArticle

@article{08d3f2bf72e148e6880c7536e2195c42,
title = "Lineage-specific patterns of functional diversification in the α-and β-globin gene families of tetrapod vertebrates",
abstract = "The α-and β-globin gene families of jawed vertebrates have diversified with respect to both gene function and the developmental timing of gene expression. Phylogenetic reconstructions of globin gene family evolution have provided suggestive evidence that the developmental regulation of hemoglobin synthesis has evolved independently in multiple vertebrate lineages. For example, the embryonic β-like globin genes of birds and placental mammals are not 1:1 orthologs. Despite the similarity in developmental expression profiles, the genes are independently derived from lineage-specific duplications of a β-globin pro-ortholog. This suggests the possibility that other vertebrate taxa may also possess distinct repertoires of globin genes that were produced by repeated rounds of lineage-specific gene duplication and divergence. Until recently, investigations into this possibility have been hindered by the dearth of genomic sequence data from nonmammalian vertebrates. Here, we report new insights into globin gene family evolution that were provided by a phylogenetic analysis of vertebrate globins combined with a comparative genomic analysis of three key sauropsid taxa: a squamate reptile (anole lizard, Anolis carolinensis), a passeriform bird (zebra finch, Taeniopygia guttata), and a galliform bird (chicken, Gallus gallus). The main objectives of this study were 1) to characterize evolutionary changes in the size and membership composition of the α-and β-globin gene families of tetrapod vertebrates and 2) to test whether functional diversification of the globin gene clusters occurred independently in different tetrapod lineages. Results of our comparative genomic analysis revealed several intriguing patterns of gene turnover in the globin gene clusters of different taxa. Lineage-specific differences in gene content were especially pronounced in the β-globin gene family, as phylogenetic reconstructions revealed that amphibians, lepidosaurs (as represented by anole lizard), archosaurs (as represented by zebra finch and chicken), and mammals each possess a distinct independently derived repertoire of β-like globin genes. In contrast to the ancient functional diversification of the α-globin gene cluster in the stem lineage of tetrapods, the physiological division of labor between early-and late-expressed genes in the β-globin gene cluster appears to have evolved independently in several tetrapod lineages.",
keywords = "Anolis, Gene duplication, Gene family evolution, Genome evolution, Hemoglobin, Zebra finch",
author = "Hoffmann, {Federico G.} and Storz, {Jay F.} and Gorr, {Thomas A.} and Opazo, {Juan C.}",
year = "2010",
month = "5",
doi = "10.1093/molbev/msp325",
language = "English (US)",
volume = "27",
pages = "1126--1138",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "5",

}

TY - JOUR

T1 - Lineage-specific patterns of functional diversification in the α-and β-globin gene families of tetrapod vertebrates

AU - Hoffmann, Federico G.

AU - Storz, Jay F.

AU - Gorr, Thomas A.

AU - Opazo, Juan C.

PY - 2010/5

Y1 - 2010/5

N2 - The α-and β-globin gene families of jawed vertebrates have diversified with respect to both gene function and the developmental timing of gene expression. Phylogenetic reconstructions of globin gene family evolution have provided suggestive evidence that the developmental regulation of hemoglobin synthesis has evolved independently in multiple vertebrate lineages. For example, the embryonic β-like globin genes of birds and placental mammals are not 1:1 orthologs. Despite the similarity in developmental expression profiles, the genes are independently derived from lineage-specific duplications of a β-globin pro-ortholog. This suggests the possibility that other vertebrate taxa may also possess distinct repertoires of globin genes that were produced by repeated rounds of lineage-specific gene duplication and divergence. Until recently, investigations into this possibility have been hindered by the dearth of genomic sequence data from nonmammalian vertebrates. Here, we report new insights into globin gene family evolution that were provided by a phylogenetic analysis of vertebrate globins combined with a comparative genomic analysis of three key sauropsid taxa: a squamate reptile (anole lizard, Anolis carolinensis), a passeriform bird (zebra finch, Taeniopygia guttata), and a galliform bird (chicken, Gallus gallus). The main objectives of this study were 1) to characterize evolutionary changes in the size and membership composition of the α-and β-globin gene families of tetrapod vertebrates and 2) to test whether functional diversification of the globin gene clusters occurred independently in different tetrapod lineages. Results of our comparative genomic analysis revealed several intriguing patterns of gene turnover in the globin gene clusters of different taxa. Lineage-specific differences in gene content were especially pronounced in the β-globin gene family, as phylogenetic reconstructions revealed that amphibians, lepidosaurs (as represented by anole lizard), archosaurs (as represented by zebra finch and chicken), and mammals each possess a distinct independently derived repertoire of β-like globin genes. In contrast to the ancient functional diversification of the α-globin gene cluster in the stem lineage of tetrapods, the physiological division of labor between early-and late-expressed genes in the β-globin gene cluster appears to have evolved independently in several tetrapod lineages.

AB - The α-and β-globin gene families of jawed vertebrates have diversified with respect to both gene function and the developmental timing of gene expression. Phylogenetic reconstructions of globin gene family evolution have provided suggestive evidence that the developmental regulation of hemoglobin synthesis has evolved independently in multiple vertebrate lineages. For example, the embryonic β-like globin genes of birds and placental mammals are not 1:1 orthologs. Despite the similarity in developmental expression profiles, the genes are independently derived from lineage-specific duplications of a β-globin pro-ortholog. This suggests the possibility that other vertebrate taxa may also possess distinct repertoires of globin genes that were produced by repeated rounds of lineage-specific gene duplication and divergence. Until recently, investigations into this possibility have been hindered by the dearth of genomic sequence data from nonmammalian vertebrates. Here, we report new insights into globin gene family evolution that were provided by a phylogenetic analysis of vertebrate globins combined with a comparative genomic analysis of three key sauropsid taxa: a squamate reptile (anole lizard, Anolis carolinensis), a passeriform bird (zebra finch, Taeniopygia guttata), and a galliform bird (chicken, Gallus gallus). The main objectives of this study were 1) to characterize evolutionary changes in the size and membership composition of the α-and β-globin gene families of tetrapod vertebrates and 2) to test whether functional diversification of the globin gene clusters occurred independently in different tetrapod lineages. Results of our comparative genomic analysis revealed several intriguing patterns of gene turnover in the globin gene clusters of different taxa. Lineage-specific differences in gene content were especially pronounced in the β-globin gene family, as phylogenetic reconstructions revealed that amphibians, lepidosaurs (as represented by anole lizard), archosaurs (as represented by zebra finch and chicken), and mammals each possess a distinct independently derived repertoire of β-like globin genes. In contrast to the ancient functional diversification of the α-globin gene cluster in the stem lineage of tetrapods, the physiological division of labor between early-and late-expressed genes in the β-globin gene cluster appears to have evolved independently in several tetrapod lineages.

KW - Anolis

KW - Gene duplication

KW - Gene family evolution

KW - Genome evolution

KW - Hemoglobin

KW - Zebra finch

UR - http://www.scopus.com/inward/record.url?scp=77951546469&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77951546469&partnerID=8YFLogxK

U2 - 10.1093/molbev/msp325

DO - 10.1093/molbev/msp325

M3 - Article

C2 - 20047955

AN - SCOPUS:77951546469

VL - 27

SP - 1126

EP - 1138

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 5

ER -