New genes originated via multiple recombinational pathways in the β-globin gene family of rodents

Molecular Biology and Evolution

Volumn 25, Issue 12, 2008, Pages 2589-2600

  Hoffmann, Federico G ^a,b   Opazo, Juan C ^a,c   Storz, Jay F ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

^b INSTITUTO CARLOS CHAGAS   (Brazil)

^c UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

Chimeric fusion genes; Gene conversion; Gene duplication; Gene family evolution; Globin genes; Hemoglobin

Indexed keywords

BETA GLOBIN;

ARTICLE; FUSION GENE; GENE CLUSTER; GENE DELETION; GENE DUPLICATION; GENE MUTATION; GENE STRUCTURE; GENETIC RECOMBINATION; MOLECULAR EVOLUTION; MOUSE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; RODENT;

ANIMALS; BETA-GLOBINS; EVOLUTION, MOLECULAR; MICE; MULTIGENE FAMILY; RATS; RECOMBINATION, GENETIC; RODENTIA;

MUROIDEA; MUS MUSCULUS; RODENTIA;

EID: 56449106384     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn200     Document Type: Article

References (71)

1. Aguileta G, Bielawski JP, Yang ZH. 2006. Proposed standard nomenclature for the alpha- and beta-globin gene families. Genes Genet Syst. 81:367-371.
2. Bulger M, Bender MA, Hikke van Doorninck J, Wertman B, Farrell CM, Felsenfeld G, Groudine M, Hardison R. 2000. Comparative structural and functional analysis of the olfactory receptor genes flanking the human and mouse β-globin gene clusters. Proc Natl Acad Sci USA. 97: 14560-14565.
3. Burge C, Karlin S. 1997. Prediction of complete gene structure in human genomic DNA. J Mol Biol. 268:78-94.
4. Collins FS, Weissman SM. 1984. The molecular genetics of human hemoglobin. Prog Nucleic Acid Res Mol Biol. 31:315-462.
5. Cooper SJB, Murphy R, Dolman G, Hussey D, Hope RM. 1996. A molecular and evolutionary study of the beta-globin gene family of the Australian marsupial Sminthopsis crassicaudata. Mol Biol Evol. 13:1012-1022.
6. Demuth JP, De Bie T, Stajich JE, Cristianini N, Hahn MW. 2006. The evolution of mammalian gene families. PLoS ONE. 1:e85.
7. Dickerson RE, Geis I. 1983. Hemoglobin: structure, function, evolution, and pathology. Menlo Park (CA): Benjamin/Cummings Publishing.
8. s haplotype. Mol Biol Evol. 2:304-320.
9. Fan C, Emerson JJ, Long M. 2008. The origin of new genes. In: Pagel M, Pomiankowski A, editors. Evolutionary genomics and proteomics. Sunderland (MA): Sinauer Associates. p. 27-43.
10. Feuk L, Carson AR, Scherer SW. 2006. Structural variation in the human genome. Nat Rev Genet. 7:85-97.
11. Fishmanlobell J, Rudin N, Haber JE. 1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol Cell Biol. 12: 1292-1303.
12. Forget BG. 2001. Molecular mechanisms of β thalassemia. In: Steinberg MH, Forget BG, Higgs DR, Nagel RL, editors. Disorders of hemoglobin: genetics, pathophysiology, and clinical management. Cambridge: Cambridge University Press. p. 252-276.
13. Fritsch E, Lawn R, Maniatis T. 1980. Molecular cloning and characterization of the human beta-like globin gene cluster. Cell. 19:959-972.
14. Garner KJ, Lingrel JB. 1988. Structural organization of the β-globin locus of B-haplotype sheep. Mol Biol Evol. 5:134-140.
15. Garner KJ, Lingrel JB. 1989. A comparison of the beta A- and beta B-globin clusters of sheep. J Mol Evol. 28:175-184.
16. 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.
17. Goodman M, Koop BF, Czelusniak J, Weiss ML. 1984. The η-globin gene: its long evolutionary history in the β-globin gene family of mammals. J Mol Biol. 180:803-823.
18. Grosveld F, van Assendelft GB, Greaves D, Kollias G. 1987. Position-independent, high-level expression of the human β-globin gene in transgenic mice. Cell. 51:975-985.
19. Hahn MW, Demuth JP, Han SG. 2007. Accelerated rate of gene gain and loss in primates. Genetics. 177:1941-1949.
20. Hahn MW, Han MV, Han SG. 2007. Gene family evolution across 12 Drosophila genomes. PLoS Genet. 3:2135-2146.
21. Hardies SC, Edgell MH, Hutchison CA. 1984. Evolution of the mammalian β-globin gene cluster. J Biol Chem. 259: 3748-3756.
22. Hardison R. 1984. Comparison of the β-like globin gene families of rabbits and humans indicates that the gene cluster 5′ ε-γ- δ-β 3′ predates the mammalian radiation. Mol Biol Evol. 1:390-410.
23. Hardison R. 1991. Evolution of globin gene families. In: Selander RK, Whittam TS, Clark AG, editors. Evolution at the molecular level. Sunderland (MA): Sinauer Associates. p. 272-289.
24. Hardison R. 1998. Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J Exp Biol. 201: 1099-1117.
25. 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.
26. Hardison R, Gelinas RE. 1986. Assignment of orthologous relationships among mammalian α-globin genes by examining flanking regions reveals a rapid rate of evolution. Mol Biol Evol. 3:243-261.
27. Hardison R, Margot JB. 1984. Rabbit globin pseudogene ψβ2 is a hybrid of δ- and β-globin sequences. Mol Biol Evol. 1:302-316.
28. 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.
29. Hardison R, Slightom JL, Gumucio DL, Goodman M, Stojanovic N, Miller W. 1997. Locus control regions of mammalian β-globin gene clusters: combining phylogenetic analyses and experimental results to gain functional insights. Gene. 205:73-94.
30. Hill A, Hardies SC, Phillips PC, Davis MG, Hutchison CA, Edgell MH. 1984. Two mouse early embryonic β-globin gene sequences: evolution of the nonadult β-globins. J Biol Chem. 259:3739-3747.
31. Hoffmann FG, Opazo JC, Storz JF. 2008. Rapid rates of lineage-specific gene duplication and deletion in the α-globin gene family. Mol Biol Evol. 25:591-602.
32. Holloway K, Lawson VE, Jeffreys AJ. 2006. Allelic recombination and de novo deletions in sperm in the human beta-globin gene region. Hum Mol Genet. 15:1099-1111.
33. Jeffreys AJ, Barrie P, Harris S, Fawcett D, Nugent Z, Boyd AC. 1982. Isolation and sequence analysis of a hybrid δ-globin pseudogene from the brown lemur. J Mol Biol. 156:487-503.
34. Jobb G, von Haeseler A, Strimmer K. 2004. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 4:18.
35. M) of opossum. Proc Natl Acad Sci USA. 85:3893-3897.
36. Koop BF, Siemieniak D, Slightom JL, Goodman M, Dunbar J, Wright PC, Simons EL. 1989. Tarsius δ- and β-globin genes: conversions, evolution, and systematics. J Biol Chem. 264: 68-79.
37. Lam KWG, Jeffreys AJ. 2007. Processes of de novo duplication of human alpha-globin genes. Proc Natl Acad Sci USA. 104: 10950-10955.
38. Lam K-W, Jeffreys A. 2006. Processes of copy-number change in human DNA: the dynamics of α-globin gene deletion. Proc Natl Acad Sci USA. 103:8921-8927.
39. Long M, Betran E, Thornton K, Wang W. 2003. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 4:865-875.
40. Loukopoulos D, Kollia P. 2001. Worldwide distribution of β thalassemia. In: Steinberg MH, Forget BG, Higgs DR, Nagel RL, editors. Disorders of hemoglobin: genetics, pathophysiology, and clinical management. Cambridge: Cambridge University Press. p. 861-877.
41. Lupski JR, Stankiewicz P. 2005. Genomic disorders: molecular mechanisms for rearrangements and conveyed phenotypes. PLoS Genet. 1:627-633.
42. Margot JB, Demers GW, Hardison R. 1989. Complete nucleotide sequence of the rabbit β-like globin gene cluster: analysis of intergenic sequences and comparison with the human β-like globin gene cluster. J Mol Biol. 205:15-40.
43. Metzenberg AB, Wurzer G, Huisman THJ, Smithies O. 1991. Homology requirements for unequal crossing over in humans. Genetics. 128:143-161.
44. Moon AM, Ley TL. 1990. Conservation of the primary structure, organization, and function of the human and mouse β-globin locus-activating regions. Proc Natl Acad Sci USA. 87: 7693-7697.
45. Murphy WJ, Eizirik E, O' Brien SJ, et al. (11 co-authors). 2001. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science. 294:2348-2351.
46. Nozawa M, Nei M. 2007. Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA. 104:7122-7127.
47. Opazo JC, Hoffmann FG, Storz JF. 2008a. Genomic evidence for independent origins of β-like globin genes in monotremes and therian mammals. Proc Natl Acad Sci USA. 105:1590-1595.
48. Opazo JC, Hoffmann FG, Storz JF. 2008b. Differential loss of embryonic globin genes during the radiation of placental mammals. Proc Natl Acad Sci USA. 105:12950-12955.
49. Ovcharenko I, Loots GG, Giardine BM, Hou MM, Ma J, Hardison RC, Stubbs L, Miller W. 2005. Mulan: multiple-sequence local alignment and visualization for studying function and evolution. Genome Res. 15:184-194.
50. Paunesku T, Stevanovic M, Radosavljevic D, Drmanac R, Crkvenjakov R. 1990. Origin of rat β-globin haplotypes containing three and five genes. Mol Biol Evol. 7:407-422.
51. Prasad AB, Allard MW, NISC Comparative Sequencing Program, Green ED. 2008. Confirming the phylogeny of mammals by use of large comparative sequence datasets. Mol Biol Evol. 25:1795-1808.
52. Prychitko T, Johnson RM, Wildman DE, Gumucio DL, Goodman M. 2005. The phylogenetic history of new world monkey β-globin reveals a platyrrhine β to δ gene conversion in the atelid ancestry. Mol Phylogenet Evol. 35:225-234.
53. Rodriguez F, Oliver JL, Marin A, Medina JR. 1990. The general stochastic model of nucleotide substitution. J Theor Biol. 142:485-501.
54. Ronquist F, Huelsenbeck JP. 2003. MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
55. Schimenti JC, Duncan CH. 1985. Structure and organization of the bovine β-globin genes. Mol Biol Evol. 2:514-525.
56. Schneider JA, Peto TEA, Boone RA, Boyce AJ, Clegg JB. 2002. Direct measurement of the male recombination fraction in the human beta-globin hot spot. Hum Mol Genet. 11:207-215.
57. Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, Smit A, NCS Program, Green ED, Hardison RC, Miller W. 2003. MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res. 31:3518-3524.
58. 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.
59. Shaw CJ, Lupski JR. 2004. Implications of human genome architecture for rearrangement-based disorders: the genomic basis for disease. Hum Mol Genet. 13:R57-R64.
60. Shehee WR, Loeb DD, Adey NB, et al. (15 co-authors). 1989. Nucleotide sequence of the BALB/c mouse β-globin complex. J Mol Biol. 205:41-62.
61. Steppan SJ, Adkins RM, Anderson J. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol. 53: 533-553.
62. Stevanovic M, Paunesku T, Radosavljevic D, Drmanac R, Crkvenjakov R. 1989. Variant chromosomal arrangement of adult β-globin genes in rat. Gene. 79:139-150.
63. 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.
64. Storz JF, Hoffmann FG, Opazo JC, Moriyama H. 2008. Adaptive functional divergence among triplicated α-globin genes in rodents. Genetics. 178:1623-1638.
65. Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW. 2007. The molecular basis of high-altitude adaptation in deer mice. PLoS Genet. 3:e45.
66. Tagle DA, Slightom JL, Jones RT, Goodman M. 1991. Concerted evolution led to high expression of a prosimian primate δ globin gene locus. J Biol Chem. 266:7469-7480.
67. Tatusova TA, Madden TL. 1999. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett. 174:247-250.
68. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
69. Townes TM, Fitzgerald MC, Lingrel JB. 1984. Triplication of a four-gene set during evolution of the goat β-globin locus produced three genes now expressed differentially during development. Proc Natl Acad Sci USA. 81:6589-6593.
70. Wood WG. 2001. Hereditary persistance of fetal hemoglobin and δβ thalassemia. In: Steinberg MH, Forget BG, Higgs DR, Nagel RL, editors. Disorders of hemoglobin: genetics, pathophysiology, and clinical management. Cambridge: Cambridge University Press. p. 356-388.
71. Zhang J, Dyer KD, Rosenberg HF. 2000. Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci USA. 97:4701-4706.