Genomic organization and gene expression of the multiple globins in Atlantic cod: Conservation of globin-flanking genes in chordates infers the origin of the vertebrate globin clusters

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Wetten, Ola F ^a,b   Nederbragt, Alexander J ^c   Wilson, Robert C ^b   Jakobsen, Kjetill S ^c   Edvardsen, Rolf B ^d   Andersen, Øivind ^a,e  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b INLAND NORWAY UNIVERSITY OF APPLIED SCIENCES   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

^d INSTITUTE OF MARINE RESEARCH   (Norway)

^e NOFIMA   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COMMON ANCESTRY; ENZYME ACTIVITY; GADOID; GENE EXPRESSION; GENOME; IMMUNE RESPONSE; OXYGEN; PHYLOGENETICS;

BRANCHIOSTOMA FLORIDAE; BRANCHIOSTOMA LANCEOLATUM; CHORDATA; CIONA INTESTINALIS; GADUS MORHUA; TELEOSTEI; VERTEBRATA;

ALPHA GLOBIN; BETA GLOBIN; GLOBIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; ATLANTIC COD; CHEMISTRY; GENETICS; MOLECULAR GENETICS; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; VERTEBRATE;

ALPHA-GLOBINS; AMINO ACID SEQUENCE; ANIMALS; BETA-GLOBINS; GADUS MORHUA; GLOBINS; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; VERTEBRATES;

EID: 77957986214     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-315     Document Type: Article

References (64)

1. Darwinian evolution in the genealogy of haemoglobin. M Goodman GW Moore G Matsuda, Nature 1975 253 603 608 10.1038/253603a0 1089897
2. Linkage of adult - and -globin genes in X. laevis and gene duplication by tetraploidization. AJ Jeffreys V Wilson D Wood JP Simons RM Kay JG Williams, Cell 1980 21 555 64 10.1016/0092-8674(80)90493-6 7407927
3. The structure and evolution of the human -globin gene family. A Efstratiadis JW Posakony T Maniatis RM Lawn C O'Connell RA Spritz JK Deriel BG Forget SM Weissman JL Slightom AE Blechl O Smithies FE Baralle CC Shoulders NJ Proudfoot, Cell 1980 21 653 668 10.1016/0092-8674(80)90429-8 6985477 (Pubitemid 10022874)
4. The chromosomal arrangement of human alpha-like globin genes: sequence homology and alpha-globin gene deletions. J Lauer CK Shen T Maniatis, Cell 1980 20 119 130 10.1016/0092-8674(80)90240-8 6446404
5. Globin genes on the move. RC Hardison, J Biol 2008 7 35 10.1186/jbiol92 19040770
6. Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the alpha globin cluster. J Flint C Tufarelli J Peden K Clark RJ Daniels R Hardison W Miller S Philipsen KC Tan-Un T McMorrow J Frampton BP Alter AM Frischauf DR Higgs, Hum Mol Genet 2001 10 371 382 10.1093/hmg/10.4.371 11157800
7. 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. D Wheeler RM Hope SJ Cooper AA Gooley RA Holland, J Mol Evol 2004 58 642 52 10.1007/s00239-004-2584-0 15461421
8. Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals. VS Patel SJ Cooper JE Deakin B Fulton T Graves WC Warren RK Wilson JA Graves, BMC Biol 2008 6 34 10.1186/1741-7007-6-34 18657265
9. 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. M Bulger JH van Doorninck N Saitoh A Telling C Farrell MA Bender G Felsenfeld R Axel M Groudine, Proc Natl Acad Sci USA 1999 96 5129 5134 10.1073/pnas.96.9.5129 10220430
10. Functional and comparative analysis of globin loci in pufferfish and humans. N Gillemans T McMorrow R Tewari AW Wai C Burgtorf D Drabek N Ventress A Langeveld D Higgs K Tan-Un F Grosveld S Philipsen, Blood 2003 101 2842 2849 10.1182/blood-2002-09-2850 12517812
11. Tail-to-tail orientation of the Atlantic salmon alpha- and beta-globin genes. A Wagner F Deryckere T McMorrow F Gannon, J Mol Evol 1994 38 28 35 10.1007/BF00175492 8151712
12. Structural organization and sequence analysis of the globin locus in Atlantic salmon. T McMorrow A Wagner F Deryckere F Gannon, DNA and Cell Biol 1996 15 407 414 10.1089/dna.1996.15.407
13. Head-to-head linkage of carp - and -globin genes. M Miyata T Aoki, Biochim Biophys Acta 1997 1354 127 133 9396629
14. Adaptive evolution of gene expression in Antarctic fishes: Divergent transcription of the 5'-to-5' linked adult 1- and -globin genes of the Antarctic teleost Notothenia coriiceps is controlled by dual promoters and intergenic enhancers. DT Lau A Saeed-Kothe SK Parker HW Detrich, Amer Zool 2001 41 113 132 10.1668/0003-1569(2001)041[0113:AEOGEI]2.0.CO;2
15. Genomic organization and developmental expression of globin genes in the teleost Oryzias latipes. K Maruyama S Yasumasu K Naruse H Mitani A Shima I Iuchi, Gene 2004 335 89 100 10.1016/j.gene.2004.03.007 15194192
16. The amphibian globin gene repertoire as revealed by the Xenopus genome. A Fuchs T Burmester T Hankeln, Cytogenet Genome Res 2006 112 296 306 10.1159/000089884 16484786
17. Analysis of an inversion within the human beta globin gene cluster. MW Jennings RW Jones WG Wood DJ Weatherall, Nucl Acids Res 1985 13 2897 2906 10.1093/nar/13.8.2897 4000967
18. Species adaptation in a protein molecule. MF Perutz, Mol Biol Evol 1983 1 1 28 6400645
19. Functional adaptation and its molecular basis in vertebrate hemoglobins, neuroglobins and cytoglobins. RE Weber A Fago, Resp Physiol Neurobiol 2004 144 141 159 10.1016/j.resp.2004.04.018 (Pubitemid 39535958)
20. Adaptations for oxygen transport: lessons from fish hemoglobins. RE Weber, Hemoglobin Function in Vertebrates, Molecular Adaptation in Extreme and Temperate Environments Milano: Springer-Verlag, Di Prisco G, Giardina B, Weber RE, 2000 23 37
21. Vertebrates without erythrocytes and blood pigment. JT Ruud, Nature 1954 173 848 850 10.1038/173848a0 13165664
22. Antarctic fish hemoglobins: Evidence for adaptive evolution at subzero temperature. L Bargelloni S Marcato T Patarnello, Proc Natl Acad Sci USA 1998 95 8670 8675 10.1073/pnas.95.15.8670 9671736
23. Tracking the evolutionary loss of hemoglobin expression by the white-blooded Antarctic icefishes. G di Prisco C Ennio SK Parker HW Detrich III, Gene 2002 295 185 191 10.1016/S0378-1119(02)00691-1 12354652
24. Evolution of globin genes of the medaka Oryzias latipes (Euteleostei; Beloniformes; Oryziinae). K Maruyama S Yasumasu I Iuchi, Mech Dev 2004 121 753 769 10.1016/j.mod.2004.03.035 15210183
25. Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. M Berenbrink P Koldkjær O Kepp AR Cossins, Science 2005 307 1752 1757 10.1126/science.1107793 15774753
26. Life under pressure: insights from electronic data-storage tags into cod swimbladder function. J van der Kooij D Righton E Strand K Michalsen V Thorsteinsson H Svedäng FC Neat S Neuenfeldt, ICES J Mar Sci 2007 64 1293 1301 10.1093/icesjms/fsm119 (Pubitemid 350075753)
27. Hemoglobin polymorphisms affect the oxygen binding properties in Atlantic cod populations. Andersen OF Wetten MC De Rosa C Andre C Carelli Alinovi M Colafranceschi O Brix A Colosimo, Proc Royal Soc B 2009 276 833 841 10.1098/rspb.2008.1529
28. Organization of a and globin gene set in the teleost Atlantic cod, Gadus morhua. K Halldorsdottir E Arnason, Biochem Genet 2009 47 817 830 10.1007/s10528-009-9280-0
29. Atlantic cod (Gadus morhua) hemoglobin genes: multiplicity and polymorphism. T Borza C Stone AK Gamperl S Bowman, BMC Genetics 2009 10 51 10.1186/1471-2156-10-51 19728884
30. Large-scale sequence analyses of Atlantic cod. SD Johansen DH Coucheron M Andreassen BO Karlsen T Furmanek TE Jorgensen A Emblem R Breines JT Nordeide T Moum AJ Nederbragt NC Stenseth KS Jakobsen, New Biotechnology 2009 25 263 271 10.1016/j.nbt.2009.03.014 19491044
31. Databases of human hemoglobin variants and other resources at the globin gene server. RC Hardison DH Chui C Riemer B Giardine H Lehväslaiho H Wajcman W Miller, Hemoglobin 2001 25 183 190 10.1081/HEM-100104027 11480780
32. A SNP/microsatellite genetic linkage map of the Atlantic cod (Gadus morhua). T Moen M Delghandi MS Wesmajervi JI Westgaard KT Fjalestad, Animal Genetics 2009 40 993 996 10.1111/j.1365-2052.2009.01938.x 19694651
33. New variants of the haemoglobins of Atlantic cod: a tool for discriminating between coastal and Arctic cod populations. UEH Fyhn O Brix G Nævdal T Johansen, ICES Mar Sci Symp 1994 198 666 670
34. Haemoglobin variation in cod: a description of new variants and their geographical distribution. Husebø AK Imsland G Nævdal, Sarsia 2004 90 1 11
35. The hemoglobin aloforms in cod (Gadus morhua L.), their functional characteristics and distribution in the populations. AK Karpov GG Novikov, J Ichthyol 1980 6 45 50
36. Temperature acclimation modulates the oxygen binding properties of the Atlantic cod (Gadus morhua L.) genotypes-HbI*1/1, HbI*1/2, and HbI*2/2 by changing the concentrations of their major hemoglobin components (results from growth studies at different temperatures). O Brix S Thorkildsen A Colosimo, Comp Biochem Physiol 2004 138A 241 251
37. The oxygen transport system in three species of the boreal fish family Gadidae. C Verde M Balesrieri D de Pascale D Pagnozzi G Lecointre G di Prisco, J Biol Chem 2006 281 22073 22084 10.1074/jbc.M513080200 16717098
38. The source of oxygen secreted into the swimbladder of cod. PF Scholander L van Dam T Enns, J Cell Comp Physiol 2005 48 517 522 10.1002/jcp.1030480310
39. Novel mechanisms of pH sensitivity in tuna hemoglobin: a structural explanation of the Root effect. T Yokoyama KT Chong G Miyazaki H Morimoto DT Shih S Unzai JR Tame SY Park, J Biol Chem 2004 279 28632 29640 10.1074/jbc.M401740200 15117955
40. High resolution crystal structure of deoxy hemoglobin from Trematomus bernacchii at different pH values: the role of histidine residues in modulating the strength of the root effect. L Mazzarella A Vergara L Vitagliano A Merlino G Bonomi S Scala C Verde G di Prisco, Proteins 2006 65 490 498 10.1002/prot.21114 16909420
41. A critical role for myoglobin in zebrafish development. DH Vlecken J Teserink EB Ott PA Sakalis RT Jaspers CP Bagowski, I J Dev Biol 2009 53 517 524 10.1387/ijdb.082651dv
42. Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebrafish (Danio rerio). B Pelster WW Burggren, Circulation Res 1996 79 358 262 8756015
43. Antimicrobial peptides derived from haemoglobin are expressed in epithelium of channel catfish (Ictalurus punctatus, Rafinesque). AJ Ullal RW Litaker EJ Noga, Dev Comp Immun 2008 32 1301 1312 10.1016/j.dci.2008.04.005
44. Maternal transfer and transcriptional onset of immune genes during ontogenesis in Atlantic cod. M Seppola H Johnsen S Mennen B Myrnes H Tveiten, Dev Comp Immunol 2009 33 1205 1211 10.1016/j.dci.2009.06.013 19577592
45. Stages of embryonic development in the Atlantic cod Gadus morhua. TE Hall P Smoth IA Johnston, J Morphology 2004 259 255 270 10.1002/jmor.10222 (Pubitemid 38319056)
46. Genomic remnants of alpha-globin genes in the hemoglobinless antarctic icefishes. E Cocca M Ratnayake-Lecamwasam SK Parker L Camardella M Ciaramella G di Prisco HW Detrich, Proc Natl Acad Sci USA 1995 92 1817 21 10.1073/pnas.92.6.1817 7892183
47. Biogeography and adaptation of Notothenioid fish: hemoglobin function and globin-gene evolution. G di Prisco JT Eastman D Giordano E Parisi C Verde, Gene 2007 398 143 155 10.1016/j.gene.2007.02.047 17553637 (Pubitemid 47068898)
48. Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part II. KH Kock, Polar Biol 2005 28 897 909 10.1007/s00300-005-0020-6 (Pubitemid 41704924)
49. Hydrophobicity patterns and biological adaptation: an exemplary case from fish hemoglobins. M Colafranceschi A Giuliani Andersen O Brix MC De Rosa B Giardina A Colosimo, OMICS 2010 14 275 281 10.1089/omi.2010.0007 20450440
50. The medaka draft genome and insights into vertebrate genome evolution. M Kasahara K Naruse S Sasaki Y Nakatani W Qu B Ahsan T Yamada Y Nagayasu K Doi Y Kasai T Jindo D Kobayashi A Shimada A Toyoda Y Kuroki A Fujiyama T Sasaki A Shimizu S Asakawa N Shimizu S Hashimoto J Yang Y Lee K Matsushima S Sugano M Sakaizumi T Narita K Ohishi S Haga F Ohta H Nomoto K Nogata T Morishita T Endo T Shin-I H Takeda S Morishita Y Kohara, Nature 2007 447 714 719 10.1038/nature05846 17554307 (Pubitemid 46889726)
51. A medaka gene map: the trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping. K Naruse M Tanaka K Mita A Shima J Postlethwaite H Mitani, Genome Res 2004 14 820 828 10.1101/gr.2004004 15078856
52. Globin genes are present in Ciona intestinalis. B Ebner T Burmester T Hankeln, Mol Biol Evol 2003 20 1521 1525 10.1093/molbev/msg164 12832645
53. The amphioxus genome and evolution of the chordate karyotype. NH Putnam T Butts DE Ferrier RF Furlong U Hellsten T Kawashima M Robinson-Rechavi E Shoguchi A Terry JK Yu EL Benito-Gutiérrez I Dubchak J Garcia-Fernndez JJ Gibson-Brown IV Grigoriev AC Horton PJ de Jong J Jurka VV Kapitonov Y Kohara Y Kuroki E Lindquist S Lucas K Osoegawa LA Pennacchio AA Salamov Y Satou T Sauka-Spengler J Schmutz T Shin-I A Toyoda M Bronner-Fraser A Fujiyama LZ Holland PW Holland N Satoh DSP Rokhsar, Nature 2008 453 1064 1072 10.1038/nature06967 18563158
54. Molecular phylogeny and divergence times of deuterostome animals. JE Blair SB Hedges, Mol Biol Evol 2005 22 2275 2284 10.1093/molbev/msi225 16049193
55. The oxygenation of the atmosphere and oceans. H Holland, Phil Trans Roy Soc B 2006 361 903 910 10.1098/rstb.2006.1838 (Pubitemid 44858908)
56. 2S-binding function in annelids from sulfide-free habitats reveals molecular adaptation driven by Darwinian positive selection. X Bailly R Leroy S Carney O Collin F Zal A Toulmond D Jollivet, Proc Natl Acad Sci USA 2003 100 5885 5890 10.1073/pnas.1037686100 12721359
57. Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates. FG Hoffmann JC Opazo JF Storz, Proc Natl Acad Sci USA 2010 107 14274 14279 10.1073/pnas.1006756107 20660759
58. Hemoglobins from bacteria to man: evolution of different patterns of gene expression. R Hardison, J Exp Biol 1998 201 1099 1117 9510523
59. Active chromatin hub of the mouse alpha-globin locus forms in a transcription factory of clustered housekeeping genes. GL Zhou L Xin W Song LJ Di G Liu XS Wu DP Liu CC Liang, Mol Cell Biol 2006 26 5096 5105 10.1128/MCB.02454-05 16782894
60. Genome sequencing in microfabricated high-density picolitre reactors. M Margulies M Egholm WE Altman S Attiya JS Bader LA Bemben J Berka MS Braverman YJ Chen Z Chen SB Dewell L Du JM Fierro XV Gomes BC Godwin W He S Helgesen CH Ho GP Irzyk SC Jando ML Alenquer TP Jarvie KB Jirage JB Kim JR Knight JR Lanza JH Leamon SM Lefkowitz M Lei J Li KL Lohman H Lu VB Makhijani KE McDade MP McKenna EW Myers E Nickerson JR Nobile R Plant BP Puc MT Ronan GT Roth GJ Sarkis JF Simons JW Simpson M Srinivasan KR Tartaro A Tomasz KA Vogt GA Volkmer SH Wang Y Wang MP Weiner P Yu RF Begley JM Rothberg, Nature 2005 437 376 380 16056220
61. Selection of reference genes for qRT-PCR examination of wild populations of Atlantic cod Gadus morhua. PA Olsvik L Søfteland KK Lie, BMC Res Notes 2008 1 47 10.1186/1756-0500-1-47 18710500
62. Quantitative real-time PCR method for detection of B-lymphocyte monoclonality by comparison of and immunoglobulin light chain expression. A Ståhlberg P man B Ridell P Mostad M Kubista, Clin Chem 2003 49 51 59 10.1373/49.1.51 12507960
63. Evaluation of candidate reference genes in Q-PCR studies of Atlantic cod (Gadus morhua) ontogeny, with emphasis on the gastrointestinal tract. Sæle A Nordgreen K Hamre PA Olsvik, Comp Biochem Physiol B 2009 152 94 101 10.1016/j.cbpb.2008.10.002 18957329
64. Mitogenomic evaluation of the historical biogeography of cichlids toward reliable dating of teleostean divergences. Y Azuma Y Kumazawa M Miya K Mabuchi M Nishida, BMC Evol Biol 2008 8 215 10.1186/1471-2148-8-215 18651942