Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals

BMC Biology

Volumn 6, Issue , 2008, Pages

  Patel, Vidushi S ^a   Cooper, Steven J B ^b,c   Deakin, Janine E ^a   Fulton, Bob ^d   Graves, Tina ^d   Warren, Wesley C ^d   Wilson, Richard K ^d   Graves, Jennifer A M ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c SOUTH AUSTRALIAN MUSEUM   (Australia)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GLOBIN; BETA GLOBIN; CYTOGLOBIN; GAMMA GLOBIN; HEMOGLOBIN; TIOPRONIN; GLOBIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; BIRD; CHROMOSOME 21; CONTROLLED STUDY; DNA FLANKING REGION; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INSERTION; GENE LOCUS; GENETIC LINKAGE; GENETIC VARIABILITY; GENOME ANALYSIS; MALE; MAMMAL; MARSUPIAL; MOLECULAR EVOLUTION; MONOTREMATE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY SYSTEM; OPEN READING FRAME; PLATYPUS; SEQUENCE HOMOLOGY; UNINDEXED SEQUENCE; ANIMAL; BACTERIAL ARTIFICIAL CHROMOSOME; BIOLOGICAL MODEL; COMPARATIVE STUDY; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; MOLECULAR CLONING; MULTIGENE FAMILY; PHYLOGENY; POLYMERASE CHAIN REACTION; PROMOTER REGION; SOUTHERN BLOTTING; TRANSPOSON;

AVES; GNATHOSTOMATA (VERTEBRATE); MAMMALIA; METATHERIA; MONOTREMATA; ORNITHORHYNCHUS ANATINUS; VERTEBRATA;

ANIMALS; BIRDS; BLOTTING, SOUTHERN; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CLONING, MOLECULAR; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GLOBINS; IN SITU HYBRIDIZATION, FLUORESCENCE; MAMMALS; MODELS, GENETIC; MULTIGENE FAMILY; PHYLOGENY; PLATYPUS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); SEQUENCE ANALYSIS, DNA;

EID: 51349122509     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-6-34     Document Type: Article

References (75)

1. Roesner A Fuchs C Hankeln T Burmester T A globin gene of ancient evolutionary origin in lower vertebrates: Evidence for two distinct globin families in animals Mol Biol Evol 2005, 22:12-20. 10.1093/molbev/ msh258 15356282
2. Fuchs C Burmester T Hankeln T The amphibian globin gene repertoire as revealed by the Xenopus genome Cytogenet Genome Res 2006, 112:296-306. 10.1159/000089884 16484786
3. Dickerson RE Geis I Hemoglobin: Structure, Function, Evolution and Pathology Menlo Park, CA: Benjamin Cummings 1983, 65-116.
4. Hentschel CC Kay RM Williams JG 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 1979, 72:350-363. 10.1016/0012-1606(79)90124-6 510792
5. Jeffreys AJ Wilson V Wood D Simons JP Kay RM Williams JG Linkage of adult alpha- and beta-globin genes in X. laevis and gene duplication by tetraploidization Cell 1980, 21:555-564. 10.1016/0092-8674(80)90493-6 7407927
6. Kay RM Harris R Patient RK Williams JG Molecular cloning of cDNA sequences coding for the major alpha- and beta-globin polypeptides of adult Xenopus laevis Nucleic Acids Res 1980, 8:2691-2707. 324114 7001356 10.1093/nar/8.12.2691
7. Pisano E Cocca E Mazzei F Ghigliotti L di Prisco G Detrich HW III Ozouf-Costaz C Mapping of alpha- and beta-globin genes on Antarctic fish chromosomes by fluorescence in situ hybridization Chromosome Res 2003, 11:633-640. 10.1023/A:1024961103663 14516071
8. Gillemans N McMorrow T Tewari R Wai AW Burgtorf C Drabek D Ventress N Langeveld A Higgs D Tan-Un K Grosveld F Philipsen S Functional and comparative analysis of globin loci in pufferfish and humans Blood 2003, 101:2842-2849. 10.1182/blood-2002-09-2850 12517812
9. Dodgson JB McCune KC Rusling DJ Krust A Engel JD Adult chicken alpha-globin genes alpha A and alpha D: No anemic shock alpha-globin exists in domestic chickens Proc Natl Acad Sci USA 1981, 78:5998-6002. 348964 6273837 10.1073/pnas.78.10.5998
10. Engel JD Dodgson JB Analysis of the adult and embryonic chicken globin genes in chromosomal DNA J Biol Chem 1978, 253:8239-8246. 711749
11. Engel JD Dodgson JB Analysis of the closely linked adult chicken alpha-globin genes in recombinant DNAs Proc Natl Acad Sci USA 1980, 77:2596-2600. 349449 6248855 10.1073/pnas.77.5.2596
12. Cooper SJ Wheeler D De Leo A Cheng JF Holland RA Marshall Graves JA Hope RM The mammalian alphaD-globin gene lineage and a new model for the molecular evolution of alpha-globin gene clusters at the stem of the mammalian radiation Mol Phylogenet Evol 2006, 38:439-448. 10.1016/ j.ympev.2005.05.014 16024261
13. Goh SH Lee YT Bhanu NV Cam MC Desper R Martin BM Moharram R Gherman RB Miller JL A newly discovered human alpha-globin gene Blood 2005, 106:1466-1472. 1895206 15855277 10.1182/blood-2005-03-0948
14. Hoffmann FG Storz JF The alphaD-globin gene originated via duplication of an embryonic alpha-like globin gene in the ancestor of tetrapod vertebrates Mol Biol Evol 2007, 24:1982-1990. 10.1093/molbev/msm127 17586601
15. Hardison RC Sawada I Cheng JF Shen CK Schmid CW A previously undetected pseudogene in the human alpha globin gene cluster Nucleic Acids Res 1986, 14:1903-1911. 339581 3952001 10.1093/nar/14.4.1903
16. Lauer J Shen CK Maniatis T The chromosomal arrangement of human alpha-like globin genes: Sequence homology and alpha-globin gene deletions Cell 1980, 20:119-130. 10.1016/0092-8674(80)90240-8 6446404
17. Orkin SH The duplicated human alpha globin genes lie close together in cellular DNA Proc Natl Acad Sci USA 1978, 75:5950-5954. 393094 282616 10.1073/pnas.75.12.5950
18. Proudfoot NJ Maniatis T The structure of a human alpha-globin pseudogene and its relationship to alpha-globin gene duplication Cell 1980, 21:537-544. 10.1016/0092-8674(80)90491-2 7407925
19. Wakefield MJ Graves JA Marsupials and monotremes sort genome treasures from junk Genome Biol 2005, 6:218. 1175948 15892878 10.1186/ gb-2005-6-5-218
20. Bininda-Emonds OR Cardillo M Jones KE MacPhee RD Beck RM Grenyer R Price SA Vos RA Gittleman JL Purvis A The delayed rise of present-day mammals Nature 2007, 446:507-512. 10.1038/nature05634 17392779
21. McMillan D Miethke P Alsop AE Rens W O'Brien P Trifonov V Veyrunes F Schatzkamer K Kremitzki CL Graves T Warren W Grutzner F Ferguson-Smith MA Graves JA Characterizing the chromosomes of the platypus (Ornithorhynchus anatinus) Chromosome Res 2007, 15:961-974. 10.1007/ s10577-007-1186-2 18185982
22. Grutzner F Rens W Tsend-Ayush E El-Mogharbel N O'Brien PC Jones RC Ferguson-Smith MA Graves JA In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes Nature 2004, 432:913-917. 10.1038/nature03021 15502814
23. Rens W Grutzner F O'brien PC Fairclough H Graves JA Ferguson-Smith MA Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution Proc Natl Acad Sci USA 2004, 101:16257-16261. 528943 15534209 10.1073/pnas.0405702101
24. Warren WC Hillier LW Marshall Graves JA Birney E Ponting CP Grutzner F Belov K Miller W Clarke L Chinwalla AT Yang SP Heger A Locke DP Miethke P Waters PD Veyrunes F Fulton L Fulton B Graves T Wallis J Puente XS Lopez-Otin C Ordonez GR Eichler EE Chen L Cheng Z Deakin JE Alsop A Thompson K Kirby P Papenfuss AT Wakefield MJ Olender T Lancet D Huttley GA Smit AF Pask A Temple-Smith P Batzer MA Walker JA Konkel MK Harris RS Whittington CM Wong ES Gemmell NJ Buschiazzo E Vargas Jentzsch IM Merkel A Schmitz J Zemann A Churakov G Kriegs JO Brosius J Murchison EP Sachidanandam R Smith C Hannon GJ Tsend-Ayush E McMillan D Attenborough R Rens W Ferguson-Smith M Lefevre CM Sharp JA Nicholas KR Ray DA Kube M Reinhardt R Pringle TH Taylor J Jones RC Nixon B Dacheux JL Niwa H Sekita Y Huang X Stark A Kheradpour P Kellis M Flicek P Chen Y Webber C Hardison R Nelson J Hallsworth-Pepin K Delehaunty K Markovic C Minx P Feng Y Kremitzki C Mitreva M Glasscock J Wylie T Wohldmann P Thiru P Nhan MN Pohl CS Smith SM Hou S Renfree MB Mardis ER Wilson RK Genome analysis of the platypus reveals unique signatures of evolution Nature 2008, 453:175-183. 10.1038/nature06936 18464734
25. Cooper SJ Hope RM Evolution and expression of a beta-like globin gene of the Australian marsupial Sminthopsis crassicaudata Proc Natl Acad Sci USA 1993, 90:11777-11781. 48067 8265626 10.1073/pnas.90.24.11777
26. Cooper SJ Murphy R Dolman G Hussey D Hope RM A molecular and evolutionary study of the beta-globin gene family of the Australian marsupial Sminthopsis crassicaudata Mol Biol Evol 1996, 13:1012-1022. 8752008
27. Koop BF Goodman M Evolutionary and developmental aspects of two hemoglobin beta-chain genes (epsilon M and beta M) of opossum Proc Natl Acad Sci USA 1988, 85(11):3893-3897. 280326 3375246 10.1073/ pnas.85.11.3893
28. Lee MH Shroff R Cooper SJ Hope R Evolution and molecular characterization of a beta-globin gene from the Australian Echidna Tachyglossus aculeatus (Monotremata) Mol Phylogenet Evol 1999, 12:205-214. 10.1006/mpev.1999.0610 10381323
29. Goodman M Koop BF Czelusniak J Weiss ML The eta-globin gene. Its long evolutionary history in the beta-globin gene family of mammals J Mol Biol 1984, 180:803-823. 10.1016/0022-2836(84)90258-4 6527390
30. Hardison R Miller W Use of long sequence alignments to study the evolution and regulation of mammalian globin gene clusters Mol Biol Evol 1993, 10:73-102. 8383794
31. Hardison RC Comparison of the beta-like globin gene families of rabbits and humans indicates that the gene cluster 5′-epsilon-gamma-delta-beta-3′ predates the mammalian radiation Mol Biol Evol 1984, 1:390-410. 6599973
32. Weatherall DJ The Structure, Organization, and Regulation of Human Genes Oxford: Oxford University Press 3 1991
33. Goodman M Czelusniak J Koop BF Tagle DA Slightom JL Globins: A case study in molecular phylogeny Cold Spring Harb Symp Quant Biol 1987, 52:875-890. 3454296
34. Reitman M Grasso JA Blumenthal R Lewit P Primary sequence, evolution, and repetitive elements of the Gallus gallus (chicken) beta-globin cluster Genomics 1993, 18:616-626. 10.1016/S0888-7543(05)80364-7 8307571
35. Wheeler D Hope R Cooper SB Dolman G Webb GC Bottema CD Gooley AA Goodman M Holland RA An orphaned mammalian beta-globin gene of ancient evolutionary origin Proc Natl Acad Sci USA 2001, 98:1101-1106. 14715 11158601 10.1073/pnas.98.3.1101
36. Wheeler D Hope RM Cooper SJ Gooley AA Holland RA Linkage of the beta-like omega-globin gene to alpha-like globin genes in an Australian marsupial supports the chromosome duplication model for separation of globin gene clusters J Mol Evol 2004, 58:642-652. 10.1007/ s00239-004-2584-0 15461421
37. Holland RA Gooley AA 2nd Characterization of the embryonic globin chains of the marsupial Tammar wallaby, Macropus eugenii Eur J Biochem 1997, 248:864-871. 10.1111/j.1432-1033.1997.00864.x 9342240
38. Andersen NA Mesch U Lovell DJ Nicol SC The effects of sex, season and hybernation on haematology and blood viscosity of free-ranging echidnas (Tachyglossus aculeatus) Can J Zool 2000, 78:174-181. 10.1139/ cjz-78-2-174
39. Bently PJ Herreid CF Schmidt-Nielsen K Respiration of a monotreme, the echidna, Tachyglossus aculeatus Am J Physiol 1967, 212:957-961. 6067227
40. Parsons RS Atwood J Guiler ER Heddle RWL Comparative studies on the blood of monotremes and marsupials. I. Haematology Comp Biochem Physiol B 1971, 39(2):203-208. 10.1016/0305-0491(71)90163-5 5119901
41. Whittaker RG Thompson EO Studies on monotreme proteins. V. Amino acid sequence of the alpha-chain of haemoglobin from the platypus, Ornithorhynchus anantinus Aust J Biol Sci 1974, 27:591-605. 4464824
42. Whittaker RG Thompson EO Studies on monotreme proteins. VI. Amino acid sequence of the beta-chain of haemoglobin from the platypus, Ornithorhynchus anatinus Aust J Biol Sci 1975, 28:353-365. 1191127
43. Thompson EO Fisher WK Whittaker RG Studies on monotreme proteins. 3. Amino acid sequence of the alpha- and beta-globin chains of the minor haemoglobin from the echidna, Tachyglossus aculeatus aculeatus Aust J Biol Sci 1973, 26:1327-1335. 4798231
44. Whittaker RG Fisher WK Thompson EO Studies on monotreme proteins. I. Amino acid sequence of the beta-chain of haemoglobin from the echidna, Tachyglossus aculeatus aculeatus Aust J Biol Sci 1972, 25:989-1004. 4663350
45. University of California Santa Cruz (UCSC) Genome Browser http://genome.ucsc.edu
46. Burge C Karlin S Prediction of complete gene structures in human genomic DNA J Mol Biol 1997, 268:78-94. 10.1006/jmbi.1997.0951 9149143
47. Yeh RF Lim LP Burge CB Computational inference of homologous gene structures in the human genome Genome Res 2001, 11:803-816. 311055 11337476 10.1101/gr.175701
48. Motamed K Bastiani C Zhang Q Bailey A Shen CK CACC box and enhancer response of the human embryonic epsilon globin promoter Gene 1993, 123:235-240. 10.1016/0378-1119(93)90129-Q 8428663
49. Kim CG Sheffery M Physical characterization of the purified CCAAT transcription factor, alpha-CP1 J Biol Chem 1990, 265:13362-13369. 2376599
50. Sabath DE Koehler KM Yang WQ Phan V Wilson J DNA-protein interactions in the proximal zeta-globin promoter: Identification of novel CCACCC- and CCAAT-binding proteins Blood Cells Mol Dis 1998, 24:183-198. 10.1006/ bcmd.1998.0185 9642099
51. Whyatt DJ deBoer E Grosveld F The two zinc finger-like domains of GATA-1 have different DNA binding specificities EMBO J 1993, 12:4993-5005. 413760 8262042
52. Gillemans N Tewari R Lindeboom F Rottier R de Wit T Wijgerde M Grosveld F Philipsen S Altered DNA-binding specificity mutants of EKLF and Sp1 show that EKLF is an activator of the beta-globin locus control region in vivo Genes Dev 1998, 12:2863-2873. 317172 9744863 10.1101/ gad.12.18.2863
53. Agarwal S Arya V Stolle CA Pradhan M A novel Indian beta-thalassemia mutation in the CACCC box of the promoter region Eur J Haematol 2006, 77:530-532. 10.1111/j.0902-4441.2006.t01-1-EJH2923.x 17042767
54. Hardison R Chao KM Adamkiewicz M Price D Jackson J Zeigler T Stojanovic N Miller W Positive and negative regulatory elements of the rabbit embryonic epsilon-globin gene revealed by an improved multiple alignment program and functional analysis DNA Seq 1993, 4:163-176. 10.3109/ 10425179309015629 8161819
55. Hardison R Slightom JL Gumucio DL Goodman M Stojanovic N Miller W Locus control regions of mammalian beta-globin gene clusters: Combining phylogenetic analyses and experimental results to gain functional insights Gene 1997, 205:73-94. 10.1016/S0378-1119(97)00474-5 9461381
56. Cooper SJ Wheeler D Hope RM Dolman G Saint KM Gooley AA Holland RA The alpha-globin gene family of an Australian marsupial, Macropus eugenii: the long evolutionary history of the theta-globin gene and its functional status in mammals J Mol Evol 2005, 60:653-664. 10.1007/ s00239-004-0247-9 15983873
57. Ensembl Genome Browser http://www.ensembl.org/index.html
58. Flint J Tufarelli C Peden J Clark K Daniels RJ Hardison R Miller W Philipsen S Tan-Un KC McMorrow T Frampton J Alter BP Frischauf AM Higgs DR Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the alpha globin cluster Hum Mol Genet 2001, 10:371-382. 10.1093/hmg/10.4.371 11157800
59. Hughes JR Cheng JF Ventress N Prabhakar S Clark K Anguita E De Gobbi M de Jong P Rubin E Higgs DR Annotation of cis-regulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences Proc Natl Acad Sci USA 2005, 102:9830-9835. 1174996 15998734 10.1073/pnas.0503401102
60. Taylor TD Noguchi H Totoki Y Toyoda A Kuroki Y Dewar K Lloyd C Itoh T Takeda T Kim DW She X Barlow KF Bloom T Bruford E Chang JL Cuomo CA Eichler E FitzGerald MG Jaffe DB LaButti K Nicol R Park HS Seaman C Sougnez C Yang X Zimmer AR Zody MC Birren BW Nusbaum C Fujiyama A Hattori M Rogers J Lander ES Sakaki Y Human chromosome 11 DNA sequence and analysis including novel gene identification Nature 2006, 440:497-500. 10.1038/nature04632 16554811
61. Bulger M van Doorninck JH Saitoh N Telling A Farrell C Bender MA Felsenfeld G Axel R Groudine M Conservation of sequence and structure flanking the mouse and human beta-globin loci: The beta-globin genes are embedded within an array of odorant receptor genes Proc Natl Acad Sci USA 1999, 96:5129-5134. 21828 10220430 10.1073/pnas.96.9.5129
62. Opazo JC Hoffmann FG Storz JF Genomic evidence for independent origins of beta-like globin genes in monotremes and therian mammals Proc Natl Acad Sci USA 2008, 105:1590-1595. 10.1073/pnas.0710531105 18216242 2234189
63. Hardison RC New views of evolution and regulation of vertebrate beta-like globin gene clusters from an orphaned gene in marsupials Proc Natl Acad Sci USA 2001, 98:1327-1329. 33376 11171947 10.1073/ pnas.98.4.1327
64. Rozen S Skaletsky H Primer3 on the WWW for general users and for biologist programmers Methods Mol Biol 2000, 132:365-386. 10547847
65. The ENCODE Project Consortium The ENCODE (ENCyclopedia Of DNA Elements) Project Science 2004, 306:636-640. 10.1126/science.1105136 15499007
66. NIH Intramural Sequencing Center (NISC) http://www.nisc.nih.gov/
67. Loots GG Ovcharenko I rVISTA 2.0: Evolutionary analysis of transcription factor binding sites Nucleic Acids Res 2004, 32(Web Server):W217-W221. 441521 15215384 10.1093/nar/gkh383
68. Swofford DL PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.0b10 Sunderland, MA: Sinauer 2002 12504223
69. Huelsenbeck JP Ronquist F MRBAYES: Bayesian inference of phylogeny Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754 11524383
70. Felsenstein J Confidence limits on phylogenies: An approach using the bootstrap Evolution 1985, 39:783-791, 10.2307/2408678
71. Posada D Crandall K Modeltest: Testing the model of DNA substitution Bioinformatics 1998, 14:817-818. 10.1093/bioinformatics/14.9.817 9918953
72. MrMTgui v1.0 http://www.genedrift.org/mtgui.php
73. Rodríguez F Oliver JF Marín A Medina JR The general stochastic model of nucleotide substitutions J Theor Biol 1990, 142:485-501. 10.1016/S0022-5193(05)80104-3 2338834
74. Yang Z Among-site rate variation and its impact on phylogenetic analyses Trends Ecol Evol 1996, 11:367-372. 10.1016/0169-5347(96)10041-0
75. Rambaut A Drummond AJ Traver v1.3 2004 http://beast.bio.ed.ac.uk/Tracer