Isolation and Sequencing of Two α-Globin Genes αAand αDin Pigeon and Evidence for Embryo-Specific Expression of the αD-Globin Gene1

Ikehara, Tsuyoshi; Eguchi, Yukinori; Kayo, Susumu; Takei, Hiroshi

doi:10.1006/bbrc.1997.6667

Cited by 13 publications

(9 citation statements)

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“…5 , supplementary table S3 , Supplementary Material online), but they have retained α D -globin genes with intact reading frames. In such taxa, HbD may still be expressed during embryonic development, as documented in domestic pigeon ( Ikehara et al 1997 ).…”

Section: Resultsmentioning

confidence: 98%

“…Both duplication events occurred in the stem lineage of tetrapods after divergence from the ancestor of lobe-finned fishes approximately 370–430 Ma ( Hoffmann and Storz 2007 ). In all tetrapods that have been examined to date, the linkage order of the three α-type globin genes reflects their temporal order of expression during development: α E -globin is exclusively expressed in larval/embryonic erythroid cells derived from the yolk sac, α D -globin is expressed in both primitive and definitive erythroid cells, and α A -globin is expressed in definitive erythroid cells during later stages of prenatal development and postnatal life ( Cirotto et al 1987 ; Ikehara et al 1997 ; Alev et al 2008 , 2009 ; Storz, Hoffmann, et al 2011 ).…”

Section: Introductionmentioning

confidence: 99%

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Gene Turnover in the Avian Globin Gene Families and Evolutionary Changes in Hemoglobin Isoform Expression

Opazo

Hoffmann

Natarajan

et al. 2014

Molecular Biology and Evolution

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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.

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Section: Resultsmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Gene Turnover in the Avian Globin Gene Families and Evolutionary Changes in Hemoglobin Isoform Expression

Opazo

Hoffmann

Natarajan

et al. 2014

Molecular Biology and Evolution

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“…This suggests that the product of  observed in birds. In the definitive erythroid cells of adult birds, the  D -chain isoform typically constitutes the minor fraction of adult Hb and the  A -chain isoform typically constitutes the major fraction, although the relative abundance of the two isoforms is quite variable among species (Borgese and Bertles, 1965;Brown and Ingram, 1974;Hiebl et al, 1987;Ikehara et al, 1997).…”

Section: Expression Of -Chain Isohbsmentioning

confidence: 99%

“…As the  D -globin gene originated via duplication of an -like globin gene that had an ancestral larval/embryonic function (Hoffmann and Storz, 2007), it may be that  possess an ortholog of  E -globin. In some species of birds, for example, the  D -globin gene is only expressed during embryonic development (Ikehara et al, 1997) whereas other species express  D -globin in both primitive and definitive erythroid cells Alev et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

Storz

Hoffmann

Opazo

et al. 2011

Journal of Experimental Biology

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SUMMARYTetrapod vertebrates possess multiple -and -like globin genes that are ontogenetically regulated, such that functionally distinct hemoglobin (Hb) isoforms are synthesized during different stages of development. The -and -like globin genes of amphibians, birds and mammals are differentially expressed during embryonic development and postnatal life, but little is known about the developmental regulation of globin gene expression in non-avian reptiles. Here we report an investigation into the developmental regulation of Hb synthesis in the green anole lizard Anolis carolinensis. We tested two hypotheses derived from comparative genomic studies of the globin gene clusters in tetrapod vertebrates. First, we tested whether the product of the Anolis  D -globin gene is incorporated into embryonic Hb, thereby performing the role that would normally be performed by the embyronic  E -globin gene (which has been deleted from the green anole genome). Second, we tested whether two 'lizard-specific' -globin paralogs have independently evolved a division of labor between an early-expressed embryonic gene and a later-expressed adult gene. Results of a proteomic analysis revealed that -and -like globin genes of the anole are differentially expressed during embryonic development. However, the same repertoire of -and -chain Hb isoforms was expressed during all stages of development and postnatal life, and the ontogenetic shifts in isoform composition were relatively subtle. In contrast to the pattern that has been documented in other tetrapod vertebrates, it appears that the developmental regulation of Hb synthesis in the green anole lizard does not involve discrete, stage-specific switches in gene activation and gene silencing.

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“…As a consequence, somewhere in crocodilian evolution (1) the ␣ D gene may have either turned into a pseudogene or been completely lost, or (2) ␣ D expression became restricted to prenatal stages [where, in fact, embryonic (HbE) and adult (HbA) hemoglobins are known not only to differ in their intrinsic functional properties but also to utilize different allosteric effectors, i.e., ATP in HbE and HCO 3 − in HbA (Grigg et al 1993)]. In correspondence with the second possibility, Ikehara et al (1997) reported an embryo-specific ␣ D expression pattern in pigeons, one of the few bird species that do not have ␣ D -globins (HbD) at the adult stage.…”

Section: Evolution Of Reptilian Hemoglobinsmentioning

confidence: 99%

Phylogenetic Analysis of Reptilian Hemoglobins: Trees, Rates, and Divergences

1998

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Phylogenetic relationships among reptiles were examined using previously published and newly determined hemoglobin sequences. Trees reconstructed from these sequences using maximum-parsimony, neighbor-joining, and maximum-likelihood algorithms were compared with a phylogenetic tree of Amniota, which was assembled on the basis of published morphological data. All analyses differentiated alpha chains into alphaA and alphaD types, which are present in all reptiles except crocodiles, where only alphaA chains are expressed. The occurrence of the alphaD chain in squamates (lizards and snakes only in this study) appears to be a general characteristic of these species. Lizards and snakes also express two types of beta chains (betaI and betaII), while only one type of beta chain is present in birds and crocodiles. Reconstructed hemoglobin trees for both alpha and beta sequences did not yield the monophyletic Archosauria (i.e., crocodilians + birds) and Lepidosauria (i.e., Sphenodon + squamates) groups defined by the morphology tree. This discrepancy, as well as some other poorly resolved nodes, might be due to substantial heterogeneity in evolutionary rates among single hemoglobin lineages. Estimation of branch lengths based on uncorrected amino acid substitutions and on distances corrected for multiple substitutions (PAM distances) revealed that relative rates for squamate alphaA and alphaD chains and crocodilian beta chains are at least twice as high as those of the rest of the chains considered. In contrast to these rate inequalities between reptilian orders, little variation was found within squamates, which allowed determination of absolute evolutionary rates for this subset of hemoglobins. Rate estimates for hemoglobins of lizards and snakes yielded 1.7 (alphaA) and 3.3 (beta) million years/PAM when calibrated with published divergence time vs. PAM distance correlates for several speciation events within snakes and for the squamate left and right arrow sphenodontid split. This suggests that hemoglobin chains of squamate reptiles evolved approximately 3.5 (alphaA) or approximately 1.7 times (beta) faster than their mammalian equivalents. These data also were used to obtain a first estimate of some intrasquamate divergence times.

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Isolation and Sequencing of Two α-Globin Genes αAand αDin Pigeon and Evidence for Embryo-Specific Expression of the αD-Globin Gene1

Cited by 13 publications

References 0 publications

Gene Turnover in the Avian Globin Gene Families and Evolutionary Changes in Hemoglobin Isoform Expression

Gene Turnover in the Avian Globin Gene Families and Evolutionary Changes in Hemoglobin Isoform Expression

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

Phylogenetic Analysis of Reptilian Hemoglobins: Trees, Rates, and Divergences

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