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

Molecular Biology and Evolution

Volumn 27, Issue 5, 2010, Pages 1126-1138

  Hoffmann, Federico G ^a,b   Storz, Jay F ^b   Gorr, Thomas A ^c   Opazo, Juan C ^d  

^a INSTITUTO CARLOS CHAGAS   (Brazil)

^b UNIVERSITY OF NEBRASKA   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

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

Indexed keywords

ALPHA GLOBIN; BETA GLOBIN;

AMPHIBIA; ANOLE LIZARD; ARTICLE; BIRD; CHICKEN; GENE CLUSTER; GENE DUPLICATION; GENE FUNCTION; GLOBIN GENE; LINE DIFFERENCE; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POEPHILA CASTANOTIS; REPTILE; VERTEBRATE;

AMPHIBIA; ANOLIS; ANOLIS CAROLINENSIS; AVES; EUTHERIA; GALLIFORMES; GALLUS GALLUS; GNATHOSTOMATA (VERTEBRATE); LEPIDOSAURIA; MAMMALIA; PASSERIFORMES; REPTILIA; SAUROPSIDA; SQUAMATA; TAENIOPYGIA GUTTATA; TETRAPODA; VERTEBRATA;

EID: 77951546469     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp325     Document Type: Article

References (83)

1. Aguileta G, Bielawski JP, Yang Z. 2004. Gene conversion and functional divergence in the b-globin gene family. J Mol Evol. 59:177-189.
2. Aguileta G, Bielawski JP, Yang Z. 2006. Evolutionary rate variation among vertebrate b-globin genes: implications for dating gene family duplication events. Gene 380:21-29.
3. Alev C, McIntyre BAS, Nagai H, Shin M, Shinmyozu K, Jakt LM, Sheng G. 2008. BetaA, the major b-globin in definitive red blood cells, is present from the onset of primitive erythropoiesis in chicken. Dev Dyn. 237:1193-1197.
4. Alev C, Shinmyozu K, McIntyre BAS, Sheng G. 2009. Genomic organization of zebra finch a-and b-globin genes and their expression in primitive and definitive blood in comparison with globins in chicken. Dev Genes Evol. 219:353-360.
5. Banville D, Williams JG. 1985a. Developmental changes in the pattern of larval b-globin gene expression in Xenopus laevis. Identification of two early larval beta-globin mRNA sequences. J Mol Biol. 184:611-620.
6. Banville D, Williams JG. 1985b. The pattern of expression of the Xenopus laevis tadpole a-globin genes and the amino acid sequence of the three major tadpole a-globin polypeptides. Nucleic Acids Res. 13:5407-5421.
7. Borgese TA, Bertles JF. 1965. Hemoglobin heterogeneity: embryonic hemoglobin in the duckling and its disappearance in the adult. Science 148:509-511.
8. Brittain T. 2002. Molecular aspects of embryonic hemoglobin function. Mol Aspects Med. 23:293-342.
9. Brown JL, Ingram VM. 1974. Structural studies on chick embryonic hemoglobins. J Biol Chem. 249:3960-3972.
10. Bruns GA, Ingram VM. 1973a. Erythropoiesis in the developing chick embryo. Dev Biol. 30:455-459.
11. Bruns GA, Ingram VM. 1973b. The erythroid cells and haemoglobins of the chick embryo. Philos Trans R Soc Lond B Biol Sci. 266:225-305.
12. Bulger M, van Doorninck JH, Saitoh N, Telling A, Farrell C, Bender MA, Felsenfeld G, Axel R, Groudine M. 1999. Conservation of sequence and structure flanking the mouse and human b-globin loci: the b-globin genes are embedded within an array of odorant receptor genes. Proc Natl Acad Sci USA. 96:5129-5134.
13. Burge C, Karlin S. 1997. Prediction of complete gene structures in human genomic DNA. J Mol Biol. 268:78-94.
14. Burmester T, Haberkamp M, Mitz S, Roesner A, Schmidt M, Ebner B, Gerlach F, Fuchs C, Hankeln T. 2004. Neuroglobin and cytoglobin: genes, proteins, and evolution. IUBMB Life. 56:703-707.
15. Chan FY, Robinson J, Brownlie A, Shivdasani RA, Donovan A, Brugnara C, Kim J, Lau BC, Witkowska HE, Zon LI. 1997. Characterization of adult a-and b-globin genes in the zebrafish. Blood 89:688-700.
16. Cheng JF, Raid L, Hardison RC. 1987. Block duplications of a zeta-zeta-alpha-theta gene set in the rabbit a-like globin gene cluster. J Biol Chem. 262:5414-5421.
17. Collins FS, Weissman SM. 1984. The molecular genetics of human hemoglobin. Prog Nucleic Acid Res Mol Biol. 31:315-462.
18. Cooper SJB, Wheeler D, De Leo A, Cheng J, Holland RAB, Marshall Graves JA, Hope RM. 2006. The mammalian aD-globin gene lineage and a new model for the molecular evolution of a-globin gene clusters at the stem of the mammalian radiation. Mol Phylogenet Evol. 38:439-448.
19. Czelusniak J, Goodman M, Hewett-Emmett D, Weiss ML, Venta PJ, Tashian RE. 1982. Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature 298:297-300.
20. De Leo AA, Wheeler D, Lefevre C, Cheng J, Hope R, Kuliwaba J, Nicholas KR, Westerman M, Graves JAM. 2005. Sequencing and mapping hemoglobin gene clusters in the Australian model dasyurid marsupial Sminthopsis macroura. Cytogenet Genome Res. 108:333-341.
21. Demuth JP, Hahn MW. 2009. The life and death of gene families. Bioessays 31:29-39.
22. Dodgson JB, Stadt SJ, Choi OR, Dolan M, Fischer HD, Engel JD. 1983. The nucleotide sequence of the embryonic chicken b-type globin genes. J Biol Chem. 258:12685-12692.
23. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
24. Flint J, Tufarelli C, Peden J, et al. (14 co-authors). 2001. Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the a-globin cluster. Hum Mol Genet. 10:371-382.
25. Fuchs C, Burmester T, Hankeln T. 2006. The amphibian globin gene repertoire as revealed by the Xenopus genome. Cytogenet Genome Res. 112:296-306.
26. Gillemans N, McMorrow T, Tewari R, et al. (12 co-authors). 2003. Functional and comparative analysis of globin loci in pufferfish and humans. Blood 101:2842-2849.
27. Goh S, Lee YT, Bhanu NV, Cam MC, Desper R, Martin BM, Moharram R, Gherman RB, Miller JL. 2005. A newly discovered human a-globin gene. Blood 106:1466-1472.
28. Goodman M, Czelusniak J, Koop BF, Tagle DA, Slightom JL. 1987. Globins: a case study in molecular phylogeny. Cold Spring Harb Symp Quant Biol. 52:875-890.
29. Goodman M, Moore GW, Matsuda G. 1975. Darwinian evolution in the genealogy of haemoglobin. Nature 253:603-608.
30. Gorr TA. 1993. Hämoglobin: Sequenz und Phylogenie. Die Primär-struktur von Globinketten des Quastenflossers (Latimeria chalumnae) sowie folgender Reptilien: Galapagos-Meerechse (Amblyrhynchus cristatus), Grüner Leguan (Iguana iguana), Indigonatter (Drymarchon corais), Glattstirnkaiman (Paleosuchus palpebrosus). [Ph.D thesis]. [Munich (Germany)]: University of Munich.
31. Gorr TA, Mable BK, Kleinschmidt T. 1998. Phylogenetic analysis of reptilian hemoglobins: trees, rates, and divergences. J Mol Evol. 47:471-485.
32. Hankeln T, Ebner B, Fuchs C, et al. (23 co-authors). 2005. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J Inorg Biochem. 99:110-119.
33. Hankeln T, Wystub S, Laufs T, Schmidt M, Gerlach F, Saaler-Reinhardt S, Reuss S, Burmester T. 2004. The cellular and subcellular localization of neuroglobin and cytoglobin-a clue to their function? IUBMB Life. 56:671-679.
34. Hardison R. 1998. Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J Exp Biol. 201:1099-1117.
35. Hardison R. 2001. Organization, evolution, and regulation of the globin genes. In: Steinberg MH, Forget BG, Higgs DR, Nagel RL, editors. Disorders of hemoglobin: genetics, pathophysiology, and clinical management. Cambridge: Cambridge University Press. p. 95-116.
36. Hardison R, Miller W. 1993. Use of long sequence alignments to study the evolution and regulation of mammalian globin gene clusters. Mol Biol Evol. 10:73-102.
37. Hardison RC. 2008. Globin genes on the move. J Biol. 7:35.
38. Hardison RC, Gelinas RE. 1986. Assignment of orthologous relationships among mammalian a-globin genes by examining flanking regions reveals a rapid rate of evolution. Mol Biol Evol. 3:243-261.
39. Hedges SB. 2009. The timetree of life. Oxford: Oxford University Press.
40. Hedges SB, Dudley J, Kumar S. 2006. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972.
41. Hentschel CC, Kay RM, Williams JG. 1979. Analysis of Xenopus laevis globins during development and erythroid cell maturation and the construction of recombinant plasmids containing sequences derived from adult globin mRNA. Dev Biol. 72:350-363.
42. Hiebl I, Braunitzer G, Schneeganss D. 1987. The primary structures of the major and minor hemoglobin-components of adult Andean goose (Chloephaga melanoptera, Anatidae): the mutation Leu/Ser in position 55 of the b-chains. Biol Chem Hoppe Seyler. 368:1559-1569.
43. Higgs DR, Vickers MA, Wilkie AO, Pretorius IM, Jarman AP, Weatherall DJ. 1989. A review of the molecular genetics of the human a-globin gene cluster. Blood 73:1081-1104.
44. Hoffmann FG, Opazo JC, Storz JF. 2008a. New genes originated via multiple recombinational pathways in the b-globin gene family of rodents. Mol Biol Evol. 25:2589-2600.
45. Hoffmann FG, Opazo JC, Storz JF. 2008b. Rapid rates of lineage-specific gene duplication and deletion in the a-globin gene family. Mol Biol Evol. 25:591-602.
46. Hoffmann FG, Storz JF. 2007. The aD-globin gene originated via duplication of an embryonic a-like globin gene in the ancestor of tetrapod vertebrates. Mol Biol Evol. 24:1982-1990.
47. Hosbach HA, Wyler T, Weber R. 1983. The Xenopus laevis globin gene family: chromosomal arrangement and gene structure. Cell 32:45-53.
48. Hughes JR, Cheng J, Ventress N, Prabhakar S, Clark K, Anguita E, De Gobbi M, de Jong P, Rubin E, Higgs DR. 2005. Annotation of cis-regulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences. Proc Natl Acad Sci USA. 102:9830-9835.
49. Ikehara T, Eguchi Y, Kayo S, Takei H. 1997. Isolation and sequencing of two a-globin genes a(A) and a(D) in pigeon and evidence for embryo-specific expression of the a(D)-globin gene. Biochem Biophys Res Commun. 234:450-453.
50. Jeffreys AJ, Wilson V, Wood D, Simons JP, Kay RM, Williams JG. 1980. Linkage of adult a-and b-globin genes in X. laevis and gene duplication by tetraploidization. Cell 21:555-564.
51. Jobb G, von Haeseler A, Strimmer K. 2004. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 4:18.
52. Kay RM, Harris R, Patient RK, Williams JG. 1980. Molecular cloning of cDNA sequences codingfor the majora-and b-globin polypeptides of adult Xenopus laevis. Nucleic Acids Res. 8:2691-2707.
53. Lynch M. 2007. The origins of genome architecture. Sunderland (MA): Sinauer Associates.
54. McIntyre BAS, Alev C, Tarui H, Jakt LM, Sheng G. 2008. Expression profiling of circulating non-red blood cells in embryonic blood BMC Dev Biol. 8:21.
55. Nagai H, Sheng G. 2008. Definitive erythropoiesis in chicken yolk sac. Dev Dyn. 237:3332-3341.
56. Nagel RL, Steinberg MH. 2001. Role of epistatic (modifier) genes in the modulation of the phenotypic diversity of sickle cell anemia. Pediatr Pathol Mol Med. 20:123-136.
57. Nakatani K, Okuyama H, Shimahara Y, Saeki S, Kim D, Nakajima Y, Seki S, Kawada N, Yoshizato K. 2004. Cytoglobin/STAP, its unique localization in splanchnic fibroblast-like cells and function in organ fibrogenesis. Lab Invest. 84:91-101.
58. Nakazawa F, Nagai H, Shin M, Sheng G. 2006. Negative regulation of primitive hematopoiesis by the FGF signaling pathway. Blood 108:3335-3343.
59. Ohno S. 1970. Evolution by gene duplication. Berlin (Germany): Springer-Verlag.
60. Opazo JC, Hoffmann FG, Storz JF. 2008a. Differential loss of embryonic globin genes during the radiation of placental mammals. Proc Natl Acad Sci USA. 105:12950-12955.
61. Opazo JC, Hoffmann FG, Storz JF. 2008b. Genomic evidence for independent origins of b-like globin genes in monotremes and therian mammals. Proc Natl Acad Sci USA. 105:1590-1595.
62. Opazo JC, Sloan AM, Campbell KL, Storz JF. 2009. Origin and ascendancy of a chimeric fusion gene: the b/d-globin gene of paenungulate mammals. Mol Biol Evol. 26:1469-1478.
63. Patel VS, Cooper SJB, Deakin JE, Fulton B, Graves T, Warren WC, Wilson RK, Graves JAM. 2008. Platypus globin genes and flanking loci suggest a new insertional model for b-globin evolution in birds and mammals. BMC Biol. 6:34.
64. Pisano E, Cocca E, Mazzei F, Ghigliotti L, di Prisco G, Detrich HW 3rd, Ozouf-Costaz C. 2003. Mapping of a-and b-globin genes on Antarctic fish chromosomes by fluorescence in-situ hybridization. Chromosome Res. 11:633-640.
65. Proudfoot NJ, Gil A, Maniatis T. 1982. The structure of the human f-globin gene and a closely linked, nearly identical pseudogene. Cell 31:553-563.
66. Reitman M, Grasso JA, Blumenthal R, Lewit P. 1993. Primary sequence, evolution, and repetitive elements of the Gallus gallus (chicken) b-globin cluster. Genomics 18:616-626. (Pubitemid 24021080)
67. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
68. Rücknagel KP, Braunitzer G, Wiesner H. 1988. Hemoglobins of reptiles. The primary structures of the a I-and b I-chains of common iguana (Iguana iguana) hemoglobin. Biol Chem Hoppe Seyler. 369:1143-1150.
69. Runck AM, Moriyama H, Storz JF. 2009. Evolution of duplicated b-globin genes and the structural basis of hemoglobin isoform differentiation in Mus. Mol Biol Evol. 26:2521-2532.
70. Schmidt M, Gerlach F, Avivi A, et al. (11 co-authors). 2004. Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J Biol Chem. 279:8063-8069.
71. Schmidt M, Laufs T, Reuss S, Hankeln T, Burmester T. 2005. Divergent distribution of cytoglobin and neuroglobin in the murine eye. Neurosci Lett. 374:207-211.
72. Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W. 2000. PipMaker\a web server for aligning two genomic DNA sequences. Genome Res. 10:577-586.
73. Steppan S, Adkins R, Anderson J. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol. 53:533-553.
74. Stoeckelhuber M. 1992. Sequenzermittlung von Schlangenhaemo-globinen. Primaerstrucktur von Globinketten der Indigonatter (Drymarchon corais erebenus) und des Tigerpython (Python molurus bivittatus). [diploma thesis]. [Munich (Germany)]: University of Munich.
75. Stoeckelhuber M, Gorr T, Kleinschmidt T. 2002. The primary structure of three hemoglobin chains from the indigo snake (Drymarchon corais erebennus, Serpentes): first evidence for aD chains and two b chain types in snakes. Biol Chem. 383:1907-1916.
76. Storz JF, Baze M, Waite JL, Hoffmann FG, Opazo JC, Hayes JP. 2007. Complex signatures of selection and gene conversion in the duplicated globin genes of house mice. Genetics 177:481-500.
77. Storz JF, Hoffmann FG, Opazo JC, Moriyama H. 2008. Adaptive functional divergence among triplicated a-globin genes in rodents. Genetics 178:1623-1638.
78. Tatusova TA, Madden TL. 1999. BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett. 174:247-250.
79. Taylor JS, Raes J. 2004. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet. 38:615-643.
80. Townes TM, Shapiro SG, Wernke SM, Lingrel JB. 1984. Duplication of a four-gene set during the evolution of the goat b-globin locus produced genes now expressed differentially in development. J Biol Chem. 259:1896-1900.
81. Wheeler D, Hope R, Cooper SB, Dolman G, Webb GC, Bottema CD, Gooley AA, Goodman M, Holland RA. 2001. An orphaned mammalian b-globin gene of ancient evolutionary origin. Proc Natl Acad Sci USA. 98:1101-1106.
82. Wheeler D, Hope RM, Cooper SJB, Gooley AA, Holland RAB. 2004. Linkage of the b-like x-globin gene to a-like globin genes in an Australian marsupial supports the chromosome duplication model for separation of globin gene clusters. J Mol Evol. 58:642-652.
83. Zhang J. 2003. Evolution by gene duplication: An update. Trends Ecol Evol. 18:292-298.