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Like Globin Genes in Monotremes and Therian Mammals

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Like Globin Genes in Monotremes and Therian Mammals Genomic evidence for independent origins of ␤-like globin genes in monotremes and therian 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 December 13, 2007 (received for review November 5, 2007) Phylogenetic reconstructions of the ␤-globin gene family in ver- embryonic ␤-globin gene is exclusively expressed in primitive tebrates have revealed that developmentally regulated systems of erythroid cells derived from the yolk sac. However, the ‘‘␧- hemoglobin synthesis have been reinvented multiple times in globin’’ gene in birds is not orthologous to the ␧-globin gene in independent lineages. For example, the functional differentiation mammals (2, 12), because they are independently derived from of embryonic and adult ␤-like globin genes occurred independently lineage-specific duplications of a proto ␤-globin gene. in birds and mammals. In both taxa, the embryonic ␤-globin gene In placental mammals (subclass Eutheria), the ␤-globin gene is exclusively expressed in primitive erythroid cells derived from cluster includes a linked set of three early expressed (prenatal) the yolk sac. However, the ‘‘␧-globin’’ gene in birds is not ortholo- genes, ␧-␥-␩,atthe5Ј end of the cluster, and a pair of late gous to the ␧-globin gene in mammals, because they are indepen- expressed (adult) genes, ␦ and ␤,atthe3Ј end. There is extensive dently derived from lineage-specific duplications of a proto variation in the copy number of these different paralogs among ␤-globin gene. Here, we report evidence that the early and late species, and in a number of placental mammal lineages, the ␩- expressed ␤-like globin genes in monotremes and therian mam- and ␦-globin genes have been inactivated or deleted (13–15). In mals (marsupials and placental mammals) are the products of marsupials (subclass Metatheria), the ␤-globin gene cluster independent duplications of a proto ␤-globin gene in each of these includes a single pair of genes, the early expressed ␧-globin gene two lineages. Results of our analysis of genomic sequence data and the late expressed ␤-globin gene (16, 17). An additional from a large number of vertebrate taxa, including sequence from ␤-like globin gene, ␻-globin, was recently discovered at the 3Ј the recently completed platypus genome, reveal that the ␧- and end of the ␣-globin gene cluster in marsupials (18–20). The ␤-globin genes of therian mammals arose via duplication of a proto location of this ‘‘orphaned’’ ␻-globin gene at the 3Ј end of the ␤ -globin gene after the therian/monotreme split. Our analysis of ␣-globin gene cluster reflects the ancestral linkage arrangement genomic sequence from the platypus also revealed the presence of of ␣- and ␤-globin genes before their translocation to different ␤ a duplicate pair of -like globin genes that originated via duplica- chromosomes. Because the ␧- and ␤-globin genes are the only ␤ tion of a proto -globin gene in the monotreme lineage. This members of the gene family that are shared between marsupials discovery provides evidence that, in different lineages of mam- and placental mammals, this single gene pair may have been ␤ mals, descendent copies of the same proto -globin gene may have inherited from the common ancestor of all mammals. Within the been independently neofunctionalized to perform physiological ␤-globin gene cluster of mammals, conservation of stage-specific tasks associated with oxygen uptake and storage during embry- expression is seen only for the embryonic ␧-globin gene, which onic development. is always located at the 5Ј end of the gene cluster in the position closest to the locus control region (LCR). The LCR is a ␤ ͉ ͉ ͉ ͉ -globin gene family platypus hemoglobin gene family evolution cis-regulatory element that is typically located 30–50 kb up- gene duplication stream of the ␧-globin gene (21–24). It appears that this prox- imity to the LCR accounts for the restriction of ␧-globin gene n most vertebrates, developmentally regulated members of the expression to embryonic erythroid cells, followed by silencing in I␣- and ␤-globin gene families direct the synthesis of function- the fetal and adult lineage of erythroid cells (25). ally distinct hemoglobin isoforms in embryonic and adult (de- In principle, comparative analysis of genomic sequence from finitive) erythroid cells. The progenitors of the ␣- and ␤-globin the platypus (Ornithorhynchus anatinus) should provide much gene families originated via tandem duplication of an ancestral, insight into the early evolution of the ␤-globin gene cluster in Ϸ single-copy globin gene 450–500 Mya in the common ancestor mammals. Because monotremes (subclass Prototheria) diverged of gnathostome vertebrates (1–3). The ancestral gene arrange- from the ancestor of therian mammals (marsupials and placental ␣ ␤ ment, consisting of a linked set of - and -like globin genes on mammals) between 231 and 217 Mya (26), comparison of the the same chromosome, has been retained in teleosts such as the genomic structure of the platypus ␤-globin gene cluster with that zebra fish (Danio rerio; ref. 4) and in amphibians such as Xenopus of therian mammals should permit inferences regarding the ␣ ␤ (5). Because the - and -globin gene clusters are located on ancestral state of the gene family at the stem of the mammalian different chromosomes in birds and mammals, the chromosomal radiation, and comparison with the avian ␤-globin gene cluster translocation that broke up the ancestral linkage arrangement should reveal which genes and genomic features are uniquely likely occurred in the common ancestor of these two vertebrate groups (6, 7). Hemoglobin synthesis is also developmentally regulated in Author contributions: J.C.O. and J.F.S. designed research; J.C.O. and F.G.H. performed some invertebrates (8), which suggests that the capacity to research; J.C.O. and F.G.H. analyzed data; and J.C.O., F.G.H., and J.F.S. wrote the paper. express functionally distinct hemoglobins at different stages of The authors declare no conflict of interest. development may have an ancient evolutionary origin (9–11). This article is a PNAS Direct Submission. However, phylogenetic reconstructions of the ␤-globin gene *Present address: Instituto de Ecologia y Evolucion, Facultad de Ciencias, Universidad family in vertebrates have revealed that developmentally regu- Austral de Chile, Casilla 567, Valdivia, Chile. lated systems of blood oxygen transport have been reinvented †To whom correspondence should be addressed. E-mail: [email protected]. multiple times in independent lineages. For example, the func- This article contains supporting information online at www.pnas.org/cgi/content/full/ tional differentiation of embryonic and adult ␤-like globin genes 0710531105/DC1. occurred independently in birds and mammals. In both taxa, the © 2008 by The National Academy of Sciences of the USA 1590–1595 ͉ PNAS ͉ February 5, 2008 ͉ vol. 105 ͉ no. 5 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0710531105 Downloaded by guest on September 26, 2021 mammalian innovations and which were inherited from the conclusion (3). The sister relationship between the 3Ј ␤-like mammalian/sauropsid ancestor. globin genes of platypus and echidna (Fig. 1) indicates that the Here, we report evidence that the early and late expressed monotreme-specific duplication occurred after divergence from ␤-like globin genes in therians and monotremes are the products the common ancestor of therian mammals. Consequently, the 5Ј of independent duplications of a proto ␤-globin gene in each of gene of monotremes is not a 1:1 ortholog of the early expressed these two lineages. Results of our analysis of genomic sequence therian ␧-globin gene, and the 3Ј gene of monotremes is not a 1:1 data from a large number of vertebrate taxa, including sequence ortholog of the late expressed therian ␤-globin gene. from the recently completed platypus genome, reveal that the ␧- and ␤-globin genes of therian mammals arose via duplication of Topology Test. To assess statistical support for our inferred a proto ␤-globin gene after the therian/monotreme split. Our scenario involving two independent duplication events in analysis of genomic sequence from the platypus also revealed the monotremes and therian mammals, we conducted a pair of presence of a duplicate pair of ␤-like globin genes that originated topology tests in which we compared our Bayesian tree (Fig. 1) via duplication of a proto ␤-globin gene in the monotreme to the topology predicted under the single-duplication model lineage. Although the 3Ј member of the duplicate gene pair and to the topology predicted under the two-duplication model. encodes the ␤-chain subunit of adult hemoglobin (27, 28), the 5Ј Under the single-duplication model, the platypus 5Ј ␤-like globin member of the duplicate gene pair has not been previously gene is placed sister to the early expressed genes of therian characterized. On the basis of positional homology with ␤-like mammals, and the monotreme (platypus and echidna) 3Ј ␤-like globin genes of other vertebrates, expression of the 5Ј gene is globin genes are placed sister to the late expressed genes of expected to be restricted to embryonic erythroid cells. This therian mammals (SI Fig. 5A). Under the two-duplication model, discovery provides evidence that, in different lineages of mam- the monophyletic clade containing all monotreme sequences is mals, descendent copies of the same proto
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