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Differential Loss of Embryonic Globin Genes During the Radiation of Placental Mammals

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Differential Loss of Embryonic Globin Genes During the Radiation of Placental Mammals Differential loss of embryonic globin genes during the radiation of placental mammals Juan C. Opazo*, Federico G. Hoffmann†, and Jay F. Storz‡ School of Biological Sciences, University of Nebraska, Lincoln, NE 68588 Edited by Morris Goodman, Wayne State University School of Medicine, Detroit, MI, and approved July 8, 2008 (received for review May 8, 2008) The differential gain and loss of genes from homologous gene eutherians) are the products of independent duplications of a proto families represents an important source of functional variation ␤-globin gene in each of these two lineages (19). Whereas the among the genomes of different species. Differences in gene ␤-globin gene cluster of marsupials has retained the ancestral content between species are primarily attributable to lineage- two-gene structure, the addition of new early- and late-expressed specific gene gains via duplication and lineage-specific losses via genes to the ␤-globin gene cluster of eutherian mammals is attrib- deletion or inactivation. Here, we use a comparative genomic utable to several successive rounds of duplication and divergence approach to investigate this process of gene turnover in the after the eutherian/marsupial split, which is thought to have oc- ␤-globin gene family of placental mammals. By analyzing genomic curred Ϸ170 Mya (20). Because the HBD gene is either weakly sequence data from representatives of each of the main superor- expressed or completely nonfunctional in the majority of eutherian dinal clades of placental mammals, we were able to reconstruct mammals, the increased functional diversity of the ␤-globin gene pathways of gene family evolution during the basal radiation of cluster in eutherian mammals is mainly attributable to the expan- this physiologically and morphologically diverse vertebrate group. sion of the ‘‘nonadult’’ HBE-HBG-HBH portion of the gene cluster. Our analysis revealed that an initial expansion of the nonadult Thanks to recent advances in the molecular systematics of portion of the ␤-globin gene cluster in the ancestor of placental eutherian mammals, we now have a solid phylogenetic framework mammals was followed by the differential loss and retention of for reconstructing pathways of gene family evolution in this mor- ancestral gene lineages, thereby generating variation in the com- phologically and physiologically diverse vertebrate group. Euther- plement of embryonic globin genes among contemporary species. ian mammals are classified into four superordinal groups: Afroth- The sorting of ␧-, ␥-, and ␩-globin gene lineages among the basal eria (which includes elephants, hyraxes, manatees, aardvarks, clades of placental mammals has produced species differences in tenrecs, and allies), Xenarthra (which includes sloths, armadillos, the functional types of hemoglobin isoforms that can be synthe- and anteaters), Laurasiatheria (which includes bats, eulipotyphlans, sized during the course of embryonic development. pangolins, carnivores, perrisodactyls, and cetartiodactyls), and Eu- archontoglires (which includes primates, tree shrews, colugos, rab- ␤-globin gene family ͉ gene duplication ͉ gene family evolution ͉ bits, and rodents). Recent phylogenomic studies have demonstrated genome evolution ͉ hemoglobin that a clade (Atlantogenata) composed of Afrotheria and Xenar- thra is the sister group of all remaining members of the eutherian crown group (Boreoeutheria) (21, 22). The inferred structure of the fforts to identify genetic changes that underlie phenotypic ␤-globin gene cluster in the common ancestor of Boreoeutheria is: differences among species traditionally focus on nucleotide E 5Ј-␧-␥-␩-␦-␤-3Ј (13, 14, 16, 23). Because the genomic structure of divergence between orthologous genes. The differential gain and the ␤-globin gene cluster has not been previously characterized in loss of genes from homologous gene families represents a less any representatives of Atlantogenata, the full complement of ␤-like widely appreciated source of functional variation among the globin genes in the crown group ancestor of eutherian mammals has genomes of different species (1–6). Differences in the comple- yet to be elucidated. ment of genes between species are primarily attributable to Here, we report the results of a comparative genomic analysis of lineage-specific gene gains via duplication and lineage-specific the ␤-globin gene cluster in a diverse set of species that encompasses losses via deletion or inactivation. The ␤-globin gene cluster of the four main superordinal clades of eutherian mammals. Results mammals represents an especially good model for investigating of our analysis demonstrate that the initial expansion of the mechanisms and processes of genome evolution, because it is one nonadult portion of the gene cluster in the ancestor of eutherian of the most intensively studied multigene families from the mammals was followed by differential retention of ancestral gene standpoint of molecular genetics and phylogenetic history (7–9). ␤ lineages among different clades, thereby generating variation in the The -globin gene cluster of mammals contains a set of devel- complement of embryonic globin genes among contemporary opmentally regulated genes that are arranged in their temporal ␧ ␥ ␩ species. By using a phylogenetic approach to reconstruct pathways order of expression (10–12). The -, -, and -globin genes of gene family evolution during the basal diversification of euther- (HBE, HBG, and HBH, respectively) are expressed in embry- ian mammals, we found that (i) all eutherian species examined have onic erythroid cells and are descended from an ancestral HBE retained an HBE gene at the 5Ј end of the cluster; (ii) most gene. The ␦- and ␤-globin genes (HBD and HBB, respectively) are expressed in fetal and adult erythroid cells and are descended from an ancestral HBB gene. There are some exceptions to these Author contributions: J.C.O. and J.F.S. designed research; J.C.O. and F.G.H. performed general patterns of stage-specific expression, because duplicated research; J.C.O. and F.G.H. analyzed data; and J.C.O. and J.F.S. wrote the paper. copies of HBG genes have been recruited for fetal expression in The authors declare no conflict of interest. anthropoid primates (8) and duplicated copies of HBB genes have This article is a PNAS Direct Submission. been recruited for exclusive fetal expression in some cetartiodactyls *Present address: Instituto de Ecologı´ay Evolucio´n, Facultad de Ciencias, Universidad Austral (13). de Chile, Casilla 567, Valdivia, Chile. In contrast to the diverse repertoire of ␤-like globin genes in †Present address: Instituto Carlos Chagas Fiocruz, Rua Prof. Algacyr Munhoz Mader 3775-CIC, eutherian (placental) mammals that have been studied to date, 81350-010, Curitiba, Brazil. monotremes and marsupials possess a single pair of ␤-like genes: an ‡To whom correspondence should be addressed. E-mail: [email protected]. early-expressed 5Ј copy and an ontogenetically later-expressed 3Ј This article contains supporting information online at www.pnas.org/cgi/content/full/ copy (14–18). Remarkably, the early- and late-expressed ␤-like 0804392105/DCSupplemental. globin genes in monotremes and therian mammals (marsupials and © 2008 by The National Academy of Sciences of the USA 12950–12955 ͉ PNAS ͉ September 2, 2008 ͉ vol. 105 ͉ no. 35 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0804392105 Downloaded by guest on October 2, 2021 Fig. 1. Genomic structure of the ␤-globin gene clus- ter in therian mammals. Phylogenetic relationships are based on a loose consensus of recent studies (21, 22, 49, 50). Diagonal slashes indicate gaps in genomic cover- age. Segments containing such gaps were not drawn to scale. The orientation of the cluster is from 5Ј (on the left) to 3Ј (on the right). representatives of Xenarthra, Afrotheria, and Euarchontoglires ␤-globin gene cluster has not been previously characterized in any have lost the HBH gene while retaining the HBG gene; and (iii) species from the former two groups. most representatives of Laurasiatheria have lost the HBG gene while retaining the HBH gene. Genomic Structure and Orthologous Relationships in Atlantogenata. Among atlantogenatan species, we obtained complete coverage of Results the ␤-globin gene cluster in one xenarthran species, the nine- Genomic Structure of the Mammalian ␤-Globin Gene Cluster. We banded armadillo, and one afrotherian species, the lesser hedgehog obtained genomic sequences that spanned the ␤-globin gene clus- tenrec. In the nonadult portion of the cluster, both species possess ters of 21 eutherian and 3 metatherian species. Comparison of the a single copy of HBE and a single copy of HBG, although HBG is ␤-globin gene clusters among the eutherian species in our study present only as a pseudogene in the armadillo (Fig. 1). We did not revealed considerable variation in the size and membership com- find a functional HBH gene in either of the atlantogenatan species position of the gene family (Fig. 1). The number of putatively examined. The only trace of HBH was a fragment (spanning intron functional genes in the cluster ranged from 2 in the pig to 8 in the 2, exon 3, and the 3Ј untranslated region) in the armadillo gene rat. As is generally the case in the globin gene clusters of vertebrates cluster that appears to be orthologous to the human HBHps (11, 12), the nonadult genes—HBE, HBH, and HBG—were lo- pseudogene (ϭ␺␩)[supporting information (SI) Fig. S1]. In the cated upstream of the late-expressed HBD and HBB genes. The adult portion of the cluster,
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