Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals

V Patel, Steven Cooper, Janine Deakin, Bob Fulton, Tina Graves, Wesley Warren, Richard Wilson, Jennifer Marshall Graves

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Background: Vertebrate alpha (a)- and beta (ß)-globin gene families exemplify the way in which genomes evolve to produce functional complexity. From tandem duplication of a single globin locus, the a- and ß-globin clusters expanded, and then were separated onto different chromosomes. The previous finding of a fossil ß-globin gene (?) in the marsupial a-cluster, however, suggested that duplication of the a-ß cluster onto two chromosomes, followed by lineage-specific gene loss and duplication, produced paralogous a- and ß-globin clusters in birds and mammals. Here we analyse genomic data from an egg-laying monotreme mammal, the platypus (Ornithorhynchus anatinus), to explore haemoglobin evolution at the stem of the mammalian radiation. Results: The platypus a-globin cluster (chromosome 21) contains embryonic and adult a- globin genes, a ß-like ?-globin gene, and the GBY globin gene with homology to cytoglobin, arranged as 5'-?-?'-aD-a3-a2-a1-?-GBY-3'. The platypus ß-globin cluster (chromosome 2) contains single embryonic and adult globin genes arranged as 5'-e-ß-3'. Surprisingly, all of these globin genes were expressed in some adult tissues. Comparison of flanking sequences revealed that all jawed vertebrate a-globin clusters are flanked by MPG-C16orf35 and LUC7L, whereas all bird and mammal ß-globin clusters are embedded in olfactory genes. Thus, the mammalian a- and ß-globin clusters are orthologous to the bird a-and ß-globin clusters respectively. Conclusion: We propose that a- and ß-globin clusters evolved from an ancient MPG-C16orf35-a-ß-GBY-LUC7L arrangement 410 million years ago. A copy of the original ß (represented by ? in marsupials and monotremes) was inserted into an array of olfactory genes before the amniote radiation (>315 million years ago), then duplicated and diverged to form orthologous clusters of ß-globin genes with different expression profiles in different lineages.
Original languageEnglish
Pages (from-to)1-22
Number of pages22
JournalBMC Biology
Volume6:34
DOIs
Publication statusPublished - 2008
Externally publishedYes

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Platypus
beta-Globins
Mammals
Globins
Birds
mammal
Genes
mammals
bird
loci
gene
birds
genes
chromosome
chromosomes
monotreme
Chromosomes
marsupial
Metatheria
Marsupialia

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Patel, V ; Cooper, Steven ; Deakin, Janine ; Fulton, Bob ; Graves, Tina ; Warren, Wesley ; Wilson, Richard ; Marshall Graves, Jennifer. / Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals. In: BMC Biology. 2008 ; Vol. 6:34. pp. 1-22.
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title = "Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals",
abstract = "Background: Vertebrate alpha (a)- and beta ({\ss})-globin gene families exemplify the way in which genomes evolve to produce functional complexity. From tandem duplication of a single globin locus, the a- and {\ss}-globin clusters expanded, and then were separated onto different chromosomes. The previous finding of a fossil {\ss}-globin gene (?) in the marsupial a-cluster, however, suggested that duplication of the a-{\ss} cluster onto two chromosomes, followed by lineage-specific gene loss and duplication, produced paralogous a- and {\ss}-globin clusters in birds and mammals. Here we analyse genomic data from an egg-laying monotreme mammal, the platypus (Ornithorhynchus anatinus), to explore haemoglobin evolution at the stem of the mammalian radiation. Results: The platypus a-globin cluster (chromosome 21) contains embryonic and adult a- globin genes, a {\ss}-like ?-globin gene, and the GBY globin gene with homology to cytoglobin, arranged as 5'-?-?'-aD-a3-a2-a1-?-GBY-3'. The platypus {\ss}-globin cluster (chromosome 2) contains single embryonic and adult globin genes arranged as 5'-e-{\ss}-3'. Surprisingly, all of these globin genes were expressed in some adult tissues. Comparison of flanking sequences revealed that all jawed vertebrate a-globin clusters are flanked by MPG-C16orf35 and LUC7L, whereas all bird and mammal {\ss}-globin clusters are embedded in olfactory genes. Thus, the mammalian a- and {\ss}-globin clusters are orthologous to the bird a-and {\ss}-globin clusters respectively. Conclusion: We propose that a- and {\ss}-globin clusters evolved from an ancient MPG-C16orf35-a-{\ss}-GBY-LUC7L arrangement 410 million years ago. A copy of the original {\ss} (represented by ? in marsupials and monotremes) was inserted into an array of olfactory genes before the amniote radiation (>315 million years ago), then duplicated and diverged to form orthologous clusters of {\ss}-globin genes with different expression profiles in different lineages.",
author = "V Patel and Steven Cooper and Janine Deakin and Bob Fulton and Tina Graves and Wesley Warren and Richard Wilson and {Marshall Graves}, Jennifer",
year = "2008",
doi = "10.1186/1741-7007-6-34",
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Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals. / Patel, V; Cooper, Steven; Deakin, Janine; Fulton, Bob; Graves, Tina; Warren, Wesley; Wilson, Richard; Marshall Graves, Jennifer.

In: BMC Biology, Vol. 6:34, 2008, p. 1-22.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals

AU - Patel, V

AU - Cooper, Steven

AU - Deakin, Janine

AU - Fulton, Bob

AU - Graves, Tina

AU - Warren, Wesley

AU - Wilson, Richard

AU - Marshall Graves, Jennifer

PY - 2008

Y1 - 2008

N2 - Background: Vertebrate alpha (a)- and beta (ß)-globin gene families exemplify the way in which genomes evolve to produce functional complexity. From tandem duplication of a single globin locus, the a- and ß-globin clusters expanded, and then were separated onto different chromosomes. The previous finding of a fossil ß-globin gene (?) in the marsupial a-cluster, however, suggested that duplication of the a-ß cluster onto two chromosomes, followed by lineage-specific gene loss and duplication, produced paralogous a- and ß-globin clusters in birds and mammals. Here we analyse genomic data from an egg-laying monotreme mammal, the platypus (Ornithorhynchus anatinus), to explore haemoglobin evolution at the stem of the mammalian radiation. Results: The platypus a-globin cluster (chromosome 21) contains embryonic and adult a- globin genes, a ß-like ?-globin gene, and the GBY globin gene with homology to cytoglobin, arranged as 5'-?-?'-aD-a3-a2-a1-?-GBY-3'. The platypus ß-globin cluster (chromosome 2) contains single embryonic and adult globin genes arranged as 5'-e-ß-3'. Surprisingly, all of these globin genes were expressed in some adult tissues. Comparison of flanking sequences revealed that all jawed vertebrate a-globin clusters are flanked by MPG-C16orf35 and LUC7L, whereas all bird and mammal ß-globin clusters are embedded in olfactory genes. Thus, the mammalian a- and ß-globin clusters are orthologous to the bird a-and ß-globin clusters respectively. Conclusion: We propose that a- and ß-globin clusters evolved from an ancient MPG-C16orf35-a-ß-GBY-LUC7L arrangement 410 million years ago. A copy of the original ß (represented by ? in marsupials and monotremes) was inserted into an array of olfactory genes before the amniote radiation (>315 million years ago), then duplicated and diverged to form orthologous clusters of ß-globin genes with different expression profiles in different lineages.

AB - Background: Vertebrate alpha (a)- and beta (ß)-globin gene families exemplify the way in which genomes evolve to produce functional complexity. From tandem duplication of a single globin locus, the a- and ß-globin clusters expanded, and then were separated onto different chromosomes. The previous finding of a fossil ß-globin gene (?) in the marsupial a-cluster, however, suggested that duplication of the a-ß cluster onto two chromosomes, followed by lineage-specific gene loss and duplication, produced paralogous a- and ß-globin clusters in birds and mammals. Here we analyse genomic data from an egg-laying monotreme mammal, the platypus (Ornithorhynchus anatinus), to explore haemoglobin evolution at the stem of the mammalian radiation. Results: The platypus a-globin cluster (chromosome 21) contains embryonic and adult a- globin genes, a ß-like ?-globin gene, and the GBY globin gene with homology to cytoglobin, arranged as 5'-?-?'-aD-a3-a2-a1-?-GBY-3'. The platypus ß-globin cluster (chromosome 2) contains single embryonic and adult globin genes arranged as 5'-e-ß-3'. Surprisingly, all of these globin genes were expressed in some adult tissues. Comparison of flanking sequences revealed that all jawed vertebrate a-globin clusters are flanked by MPG-C16orf35 and LUC7L, whereas all bird and mammal ß-globin clusters are embedded in olfactory genes. Thus, the mammalian a- and ß-globin clusters are orthologous to the bird a-and ß-globin clusters respectively. Conclusion: We propose that a- and ß-globin clusters evolved from an ancient MPG-C16orf35-a-ß-GBY-LUC7L arrangement 410 million years ago. A copy of the original ß (represented by ? in marsupials and monotremes) was inserted into an array of olfactory genes before the amniote radiation (>315 million years ago), then duplicated and diverged to form orthologous clusters of ß-globin genes with different expression profiles in different lineages.

U2 - 10.1186/1741-7007-6-34

DO - 10.1186/1741-7007-6-34

M3 - Article

VL - 6:34

SP - 1

EP - 22

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

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