Regulatory divergence of the duplicated chromosomal loci sox11a/b by subpartitioning and sequence evolution of enhancers in zebrafish

Molecular Genetics and Genomics

Volumn 283, Issue 2, 2010, Pages 171-184

  Navratilova, Pavla ^a   Fredman, David ^a,c   Lenhard, Boris ^a   Becker, Thomas S ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

Conserved synteny; Enhancer; Genomic regulatory block; ID2; RNF144A

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE; GENE DUPLICATION; GENE LOCUS; GENE SEQUENCE; GENETIC CODE; GENOME; IN SITU HYBRIDIZATION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; SOX11A GENE; SOX11B GENE; ZEBRA FISH; ANIMAL; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HUMAN; PRENATAL DEVELOPMENT; TRANSGENIC ANIMAL;

DANIO RERIO;

SOX11A PROTEIN, ZEBRAFISH; SOX11B PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR SOX; ZEBRAFISH PROTEIN;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETIC VARIATION; HUMANS; SOX TRANSCRIPTION FACTORS; SOXC TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 75649100190     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-009-0503-1     Document Type: Article

References (59)

1. SF Altschul W Gish W Miller EW Myers DJ Lipman 1990 Basic local alignment search tool J Mol Biol 215 403 410 2231712 1:CAS:528:DyaK3MXitVGmsA%3D%3D
2. TS Becker B Lenhard 2007 The random versus fragile breakage models of chromosome evolution: a matter of resolution Mol Genet Genomics 278 487 491 10.1007/s00438-007-0287-0 17851692 1:CAS:528:DC%2BD2sXhtFGrsrbE (Pubitemid 47568710)
3. G Bejerano M Pheasant I Makunin S Stephen WJ Kent JS Mattick D Haussler 2004 Ultraconserved elements in the human genome Science 304 1321 1325 10.1126/science.1098119 15131266 1:CAS:528:DC%2BD2cXkt1Ggu7k%3D (Pubitemid 38697428)
4. M Bergsland M Werme M Malewicz T Perlmann J Muhr 2006 The establishment of neuronal properties is controlled by Sox4 and Sox11 Genes Dev 20 3475 3486 10.1101/gad.403406 17182872 1:CAS:528:DC%2BD2sXhs1ejtA%3D%3D (Pubitemid 44969164)
5. J Castresana 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis Mol Biol Evol 17 540 552 10742046 1:CAS:528:DC%2BD3cXisVSgt7g%3D
6. J Cooke MA Nowak M Boerlijst J Maynard-Smith 1997 Evolutionary origins and maintenance of redundant gene expression during metazoan development Trends Genet 13 360 364 10.1016/S0168-9525(97)01233-X 9287491 1:CAS:528: DyaK2sXlslyjt70%3D (Pubitemid 27376676)
7. E de la Calle-Mustienes CG Feijoo M Manzanares JJ Tena E Rodriguez-Seguel A Letizia ML Allende JL Gomez-Skarmeta 2005 A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate Iroquois cluster gene deserts Genome Res 15 1061 1072 10.1101/gr.4004805 1:CAS:528: DC%2BD2MXotFaht7g%3D (Pubitemid 41126861)
8. S de Martino YL Yan T Jowett JH Postlethwait ZM Varga A Ashworth CA Austin 2000 Expression of sox11 gene duplicates in zebrafish suggests the reciprocal loss of ancestral gene expression patterns in development Dev Dyn 217 279 292 10.1002/(SICI)1097-0177(200003)217:3<279::AID-DVDY6>3.0.CO;2-S 10741422 (Pubitemid 30131993)
9. I Dubchak DV Ryaboy 2006 VISTA family of computational tools for comparative analysis of DNA sequences and whole genomes Methods Mol Biol 338 69 89 16888351 1:CAS:528:DC%2BD28XksFOqur8%3D
10. RC Edgar 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res 32 1792 1797 10.1093/nar/gkh340 15034147 1:CAS:528:DC%2BD2cXisF2ks7w%3D (Pubitemid 38832724)
11. S Ellingsen MA Laplante M Konig H Kikuta T Furmanek EA Hoivik TS Becker 2005 Large-scale enhancer detection in the zebrafish genome Development 132 3799 3811 10.1242/dev.01951 16049110 1:CAS:528:DC%2BD2MXhtFSrtrjF (Pubitemid 41410246)
12. PG Engstrom SJ Ho Sui O Drivenes TS Becker B Lenhard 2007 Genomic regulatory blocks underlie extensive microsynteny conservation in insects Genome Res 17 1898 1908 10.1101/gr.6669607 17989259 1:CAS:528:DC%2BD2sXhsVGhsLnF (Pubitemid 351360012)
13. PG Engstrom D Fredman B Lenhard 2008 Ancora: a web resource for exploring highly conserved noncoding elements and their association with developmental regulatory genes Genome Biol 9 R34 10.1186/gb-2008-9-2-r34 18279518 1:CAS:528:DC%2BD1cXjvVWkurs%3D (Pubitemid 351943995)
14. R Ertzer F Muller Y Hadzhiev S Rathnam N Fischer S Rastegar U Strahle 2007 Cooperation of sonic hedgehog enhancers in midline expression Dev Biol 301 578 589 10.1016/j.ydbio.2006.11.004 17157288 1:CAS:528:DC%2BD2sXls1Citg%3D%3D (Pubitemid 46073986)
15. S Fisher EA Grice RM Vinton SL Bessling A Urasaki K Kawakami AS McCallion 2006 Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish Nat Protoc 1 1297 1305 10.1038/nprot.2006.230 17406414 1:CAS:528:DC%2BD28XhtFOitLvI
16. P Flicek BL Aken K Beal B Ballester M Caccamo Y Chen L Clarke G Coates F Cunningham T Cutts T Down SC Dyer T Eyre S Fitzgerald J Fernandez-Banet S Graf S Haider M Hammond R Holland KL Howe K Howe N Johnson A Jenkinson A Kahari D Keefe F Kokocinski E Kulesha D Lawson I Longden K Megy P Meidl B Overduin A Parker B Pritchard A Prlic S Rice D Rios M Schuster I Sealy G Slater D Smedley G Spudich S Trevanion AJ Vilella J Vogel S White M Wood E Birney T Cox V Curwen R Durbin XM Fernandez-Suarez J Herrero TJ Hubbard A Kasprzyk G Proctor J Smith A Ureta-Vidal S Searle 2008 Ensembl 2008 Nucleic Acids Res 36 D707 D714 10.1093/nar/gkm988 18000006 1:CAS:528:DC%2BD1cXhtVWju7w%3D (Pubitemid 351149811)
17. A Force M Lynch FB Pickett A Amores YL Yan J Postlethwait 1999 Preservation of duplicate genes by complementary, degenerative mutations Genetics 151 1531 1545 10101175 1:CAS:528:DyaK1MXisV2rs7o%3D
18. Y Hadzhiev M Lang R Ertzer A Meyer U Strahle F Muller 2007 Functional diversification of sonic hedgehog paralog enhancers identified by phylogenomic reconstruction Genome Biol 8 R106 10.1186/gb-2007-8-6-r106 17559649 1:CAS:528:DC%2BD2sXos1SjsLc%3D (Pubitemid 351903175)
19. S Hoegg H Brinkmann JS Taylor A Meyer 2004 Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish J Mol Evol 59 190 203 10.1007/s00239-004-2613-z 15486693 1:CAS:528:DC%2BD2cXntlCkurg%3D (Pubitemid 39128342)
20. TJ Hubbard BL Aken S Ayling B Ballester K Beal E Bragin S Brent Y Chen P Clapham L Clarke G Coates S Fairley S Fitzgerald J Fernandez-Banet L Gordon S Graf S Haider M Hammond R Holland K Howe A Jenkinson N Johnson A Kahari D Keefe S Keenan R Kinsella F Kokocinski E Kulesha D Lawson I Longden K Megy P Meidl B Overduin A Parker B Pritchard D Rios M Schuster G Slater D Smedley W Spooner G Spudich S Trevanion A Vilella J Vogel S White S Wilder A Zadissa E Birney F Cunningham V Curwen R Durbin XM Fernandez-Suarez J Herrero A Kasprzyk G Proctor J Smith S Searle P Flicek 2009 Ensembl 2009 Nucleic Acids Res 37 D690 D697 10.1093/nar/gkn828 19033362 1:CAS:528:DC%2BD1cXhsFejtb%2FI
21. O Jaillon JM Aury F Brunet JL Petit N Stange-Thomann E Mauceli L Bouneau C Fischer C Ozouf-Costaz A Bernot S Nicaud D Jaffe S Fisher G Lutfalla C Dossat B Segurens C Dasilva M Salanoubat M Levy N Boudet S Castellano V Anthouard C Jubin V Castelli M Katinka B Vacherie C Biemont Z Skalli L Cattolico J Poulain V De Berardinis C Cruaud S Duprat P Brottier JP Coutanceau J Gouzy G Parra G Lardier C Chapple KJ McKernan P McEwan S Bosak M Kellis JN Volff R Guigo MC Zody J Mesirov K Lindblad-Toh B Birren C Nusbaum D Kahn M Robinson-Rechavi V Laudet V Schachter F Quetier W Saurin C Scarpelli P Wincker ES Lander J Weissenbach H Roest Crollius 2004 Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Nature 431 946 957 10.1038/nature03025 15496914 (Pubitemid 39434410)
22. MP Jankowski PK Cornuet S McIlwrath HR Koerber KM Albers 2006 SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth Neuroscience 143 501 514 10.1016/j.neuroscience.2006.09.010 17055661 1:CAS:528:DC%2BD28Xht1agt7rK (Pubitemid 44724937)
23. D Karolchik R Baertsch M Diekhans TS Furey A Hinrichs YT Lu KM Roskin M Schwartz CW Sugnet DJ Thomas RJ Weber D Haussler WJ Kent 2003 The UCSC Genome Browser Database Nucleic Acids Res 31 51 54 10.1093/nar/gkg129 12519945 1:CAS:528:DC%2BD3sXhvFSgu7g%3D (Pubitemid 36150331)
24. H Kikuta D Fredman S Rinkwitz B Lenhard TS Becker 2007 Retroviral enhancer detection insertions in zebrafish combined with comparative genomics reveal genomic regulatory blocks-a fundamental feature of vertebrate genomes Genome Biol 8 Suppl 1 S4 10.1186/gb-2007-8-s1-s4 18047696 (Pubitemid 351936428)
25. H Kikuta M Laplante P Navratilova AZ Komisarczuk PG Engstrom D Fredman A Akalin M Caccamo I Sealy K Howe J Ghislain G Pezeron P Mourrain S Ellingsen AC Oates C Thisse B Thisse I Foucher B Adolf A Geling B Lenhard TS Becker 2007 Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates Genome Res 17 545 555 10.1101/gr.6086307 17387144 1:CAS:528:DC%2BD2sXltF2isbY%3D (Pubitemid 46715504)
26. DA Kleinjan RM Bancewicz P Gautier R Dahm HB Schonthaler G Damante A Seawright AM Hever PL Yeyati V van Heyningen P Coutinho 2008 Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence PLoS Genet 4 e29 10.1371/journal.pgen.0040029 18282108 1:CAS:528:DC%2BD1cXksFeksLc%3D (Pubitemid 351328536)
27. T Kotani S Nagayoshi A Urasaki K Kawakami 2006 Transposon-mediated gene trapping in zebrafish Methods 39 199 206 10.1016/j.ymeth.2005.12.006 16814563 1:CAS:528:DC%2BD28XotFWrs7o%3D (Pubitemid 44189875)
28. S Kumar M Nei J Dudley K Tamura 2008 MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences Brief Bioinform 9 299 306 10.1093/bib/bbn017 18417537 1:CAS:528:DC%2BD1cXpt1artrg%3D (Pubitemid 351890826)
29. M Laplante H Kikuta M Konig TS Becker 2006 Enhancer detection in the zebrafish using pseudotyped murine retroviruses Methods 39 189 198 10.1016/j.ymeth.2006.01.003 16887366 1:CAS:528:DC%2BD28XotFWrs70%3D (Pubitemid 44189884)
30. T MacCarthy A Bergman 2007 The limits of subfunctionalization BMC Evol Biol 7 213 10.1186/1471-2148-7-213 17988397 1:CAS:528:DC%2BD1cXhtVSiu7Y%3D (Pubitemid 351169907)
31. A Meng H Tang BA Ong MJ Farrell S Lin 1997 Promoter analysis in living zebrafish embryos identifies a cis-acting motif required for neuronal expression of GATA-2 Proc Natl Acad Sci USA 94 6267 6272 10.1073/pnas.94.12.6267 9177206 1:CAS:528:DyaK2sXjvFCltLk%3D (Pubitemid 27270673)
32. M Muffato HR Crollius 2008 Paleogenomics in vertebrates, or the recovery of lost genomes from the mist of time Bioessays 30 122 134 10.1002/bies.20707 18200550 (Pubitemid 351196947)
33. JH Nadeau D Sankoff 1997 Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution Genetics 147 1259 1266 9383068 1:STN:280:DyaK1c%2FktlCitA%3D%3D
34. P Navratilova TS Becker 2009 Genomic regulatory blocks in vertebrates and implications in human disease Brief Funct Genomic Proteomic 8 4 333 342 10.1093/bfgp/elp019 19561171
35. P Navratilova D Fredman TA Hawkins K Turner B Lenhard TS Becker 2009 Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes Dev Biol 327 526 540 10.1016/j.ydbio.2008.10.044 19073165 1:CAS:528:DC%2BD1MXis1aqt7Y%3D
36. S Ohno 1973 Ancient linkage groups and frozen accidents Nature 244 259 262 10.1038/244259a0
37. E Oxtoby T Jowett 1993 Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development Nucleic Acids Res 21 1087 1095 10.1093/nar/21.5.1087 8464695 1:CAS:528:DyaK3sXkt1Cqs7k%3D
38. LA Pennacchio N Ahituv AM Moses S Prabhakar MA Nobrega M Shoukry S Minovitsky I Dubchak A Holt KD Lewis I Plajzer-Frick J Akiyama S De Val V Afzal BL Black O Couronne MB Eisen A Visel EM Rubin 2006 In vivo enhancer analysis of human conserved non-coding sequences Nature 444 499 502 10.1038/nature05295 17086198 1:CAS:528:DC%2BD28Xht1aku7%2FE (Pubitemid 44809068)
39. JH Postlethwait IG Woods P Ngo-Hazelett YL Yan PD Kelly F Chu H Huang A Hill-Force WS Talbot 2000 Zebrafish comparative genomics and the origins of vertebrate chromosomes Genome Res 10 1890 1902 10.1101/gr.164800 11116085 1:CAS:528:DC%2BD3MXhtF0%3D (Pubitemid 32049135)
40. VE Prince FB Pickett 2002 Splitting pairs: the diverging fates of duplicated genes Nat Rev Genet 3 827 837 10.1038/nrg928 12415313 1:CAS:528:DC%2BD38Xotlersb0%3D (Pubitemid 35303515)
41. S Rastegar I Hess T Dickmeis JC Nicod R Ertzer Y Hadzhiev WG Thies G Scherer U Strahle 2008 The words of the regulatory code are arranged in a variable manner in highly conserved enhancers Dev Biol 318 366 377 10.1016/j.ydbio.2008.03.034 18455719 1:CAS:528:DC%2BD1cXmsFKrt7c%3D
42. A Sandelin P Bailey S Bruce PG Engstrom JM Klos WW Wasserman J Ericson B Lenhard 2004 Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes BMC Genomics 5 99 10.1186/1471-2164-5- 99 15613238 1:CAS:528:DC%2BD2MXht1Okt7w%3D (Pubitemid 41357634)
43. S Schwartz WJ Kent A Smit Z Zhang R Baertsch RC Hardison D Haussler W Miller 2003 Human-mouse alignments with BLASTZ Genome Res 13 103 107 10.1101/gr.809403 12529312 1:CAS:528:DC%2BD3sXnvFGlsg%3D%3D
44. A Sidow 1996 Gen(om)e duplications in the evolution of early vertebrates Curr Opin Genet Dev 6 715 722 10.1016/S0959-437X(96)80026-8 8994842 1:CAS:528:DyaK2sXhsVWjsw%3D%3D (Pubitemid 27010631)
45. E Sock SD Rettig J Enderich MR Bosl ER Tamm M Wegner 2004 Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling Mol Cell Biol 24 6635 6644 10.1128/MCB.24.15.6635-6644. 2004 15254231 1:CAS:528:DC%2BD2cXmtlKltb8%3D (Pubitemid 38944343)
46. C Stigloher J Ninkovic M Laplante A Geling B Tannhauser S Topp H Kikuta TS Becker C Houart L Bally-Cuif 2006 Segregation of telencephalic and eye-field identities inside the zebrafish forebrain territory is controlled by Rx3 Development 133 2925 2935 10.1242/dev.02450 16818451 1:CAS:528: DC%2BD28XovFKrtLg%3D (Pubitemid 44314270)
47. AR Subramanian M Kaufmann B Morgenstern 2008 DIALIGN-TX: greedy and progressive approaches for segment-based multiple sequence alignment Algorithms Mol Biol 3 6 10.1186/1748-7188-3-6 18505568 1:CAS:528:DC%2BD1cXhtVCjtLfN (Pubitemid 351891446)
48. XH Sun NG Copeland NA Jenkins D Baltimore 1991 Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins Mol Cell Biol 11 5603 5611 1922066 1:CAS:528:DyaK38XmsVOhu78%3D
49. F Tajima 1993 Simple methods for testing the molecular evolutionary clock hypothesis Genetics 135 599 607 8244016 1:CAS:528:DyaK2cXlt1yhtbw%3D
50. JS Taylor I Braasch T Frickey A Meyer Y Van de Peer 2003 Genome duplication, a trait shared by 22000 species of ray-finned fish Genome Res 13 382 390 10.1101/gr.640303 12618368 1:CAS:528:DC%2BD3sXit1Wgtrc%3D (Pubitemid 36395395)
51. Y Van de Peer JS Taylor I Braasch A Meyer 2001 The ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes J Mol Evol 53 436 446 10.1007/s002390010233 11675603 1:CAS:528: DC%2BD3MXotVahsrw%3D (Pubitemid 32889551)
52. B Venkatesh EF Kirkness YH Loh AL Halpern AP Lee J Johnson N Dandona LD Viswanathan A Tay JC Venter RL Strausberg S Brenner 2007 Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome PLoS Biol 5 e101 10.1371/journal.pbio.0050101 17407382 1:CAS:528:DC%2BD2sXksFSmtLo%3D (Pubitemid 46631868)
53. JB Walsh 1995 How often do duplicated genes evolve new functions? Genetics 139 421 428 7705642 1:STN:280:DyaK2M3itVKrsg%3D%3D
54. IG Woods PD Kelly F Chu P Ngo-Hazelett YL Yan H Huang JH Postlethwait WS Talbot 2000 A comparative map of the zebrafish genome Genome Res 10 1903 1914 10.1101/gr.10.12.1903 11116086 1:CAS:528:DC%2BD3MXht1Y%3D (Pubitemid 32049136)
55. IG Woods C Wilson B Friedlander P Chang DK Reyes R Nix PD Kelly F Chu JH Postlethwait WS Talbot 2005 The zebrafish gene map defines ancestral vertebrate chromosomes Genome Res 15 1307 1314 10.1101/gr.4134305 16109975 1:CAS:528:DC%2BD2MXpvF2lsLk%3D (Pubitemid 41247922)
56. A Woolfe G Elgar 2007 Comparative genomics using Fugu reveals insights into regulatory subfunctionalization Genome Biol 8 R53 10.1186/gb-2007-8-4-r53 17428329 1:CAS:528:DC%2BD2sXmtV2ntbs%3D (Pubitemid 351859209)
57. A Woolfe M Goodson DK Goode P Snell GK McEwen T Vavouri SF Smith P North H Callaway K Kelly K Walter I Abnizova W Gilks YJ Edwards JE Cooke G Elgar 2005 Highly conserved non-coding sequences are associated with vertebrate development PLoS Biol 3 e7 10.1371/journal.pbio.0030007 15630479 1:CAS:528: DC%2BD2MXptVOisg%3D%3D (Pubitemid 40318113)
58. A Wurm E Sock R Fuchshofer M Wegner ER Tamm 2008 Anterior segment dysgenesis in the eyes of mice deficient for the high-mobility-group transcription factor Sox11 Exp Eye Res 86 895 907 10.1016/j.exer.2008.03.004 18423449 1:CAS:528:DC%2BD1cXmvFaruro%3D
59. RP Zinzen C Girardot J Gagneur M Braun EE Furlong 2009 Combinatorial binding predicts spatio-temporal cis-regulatory activity Nature 462 65 70 10.1038/nature08531 19890324 1:CAS:528:DC%2BD1MXhtlKktL7K