Skip to main content
SpringerLink
Log in

Clustering of Genes Coding for DNA Binding Proteins in a Regionof Atypical Evolution of the Human Genome

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Comparison of the human and mouse genomes has revealed that significant variations in evolutionary rates exist among genomic regions and that a large part of this variation is interchromosomal. We confirm in this work, using a large collection of introns, that human chromosome 19 is the one that shows the highest divergence with respect to mouse. To search for other differences among chromosomes, we examine the distribution of gene functions in human and mouse chromosomes using the Gene Ontology definitions. We found by correspondence analysis that among the strongest clusterings of gene functions in human chromosomes is a group of genes coding for DNA binding proteins in chromosome 19. Interestingly, chromosome 19 also has a very high GC content, a feature that has been proposed to promote an opening of the chromatin, thereby facilitating binding of proteins to the DNA helix. In the mouse genome, however, a similar aggregation of genes coding for DNA binding proteins and high GC content cannot be found. This suggests that the distribution of genes coding for DNA binding proteins and the variations of the chromatin accessibility to these proteins are different in the human and mouse genomes. It is likely that the overall high synonymous and intron rates in chromosome 19 are a by-product of the high GC content of this chromosome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • C Anselmi G Bocchinfuso P Santis ParticleDe M Savino A Scipioni (2000) ArticleTitleA theoretical model for the prediction of sequence-dependent nucleosome thermodynamic stability Biophys J 79 601–613 Occurrence Handle1:CAS:528:DC%2BD3cXlsFOgt7k%3D Occurrence Handle10919995

    CAS  PubMed  Google Scholar 

  • G Bernardi (2000a) ArticleTitleThe compositional evolution of vertebrate genomes Gene 259 31–43 Occurrence Handle10.1016/S0378-1119(00)00441-8 Occurrence Handle1:CAS:528:DC%2BD3MXitV2msg%3D%3D

    Article  CAS  Google Scholar 

  • G Bernardi (2000b) ArticleTitleIsochores and the evolutionary genomics of vertebrates Gene 241 3–17 Occurrence Handle10.1016/S0378-1119(99)00485-0 Occurrence Handle1:CAS:528:DyaK1MXotVGksrw%3D

    Article  CAS  Google Scholar 

  • H Caron B Schaik Particlevan M Mee Particlevan der F Baas G Riggins P Sluis Particlevan MC Hermus R Asperen Particlevan K Boon PA Voute S Heisterkamp A Kampen Particlevan R Versteeg (2001) ArticleTitleThe human transcriptome map: clustering of highly expressed genes in chromosomal domains Science 291 1289–1292 Occurrence Handle10.1126/science.1056794 Occurrence Handle1:CAS:528:DC%2BD3MXhtlSgs70%3D Occurrence Handle11181992

    Article  CAS  PubMed  Google Scholar 

  • D Casane S Boissinot BH Chang LC Shimmin W Li (1997) ArticleTitleMutation pattern variation among regions of the primate genome J Mol Evol 45 216–226 Occurrence Handle1:CAS:528:DyaK2sXms1Cru7c%3D Occurrence Handle9302314

    CAS  PubMed  Google Scholar 

  • J Castresana (2000) ArticleTitleSelection of conserved blocks from multiple alignments for their use in phylogenetic analysis Mol Biol Evol 7 540–552

    Google Scholar 

  • J Castresana (2002a) Estimation of genetic distances from human and mouse introns. Genome Biol 3:research0028.0021-0028.0027 . .

    Google Scholar 

  • J Castresana (2002b) ArticleTitleGenes on human chromosome 19 show extreme divergence from the mouse orthologues and a high GC content Nucleic Acids Res 30 1751–1756 Occurrence Handle10.1093/nar/30.8.1751 Occurrence Handle1:CAS:528:DC%2BD38Xjt1Ghsb0%3D

    Article  CAS  Google Scholar 

  • M Clamp D Andrews D Barker P Bevan G Cameron Y Chen L Clark T Cox J Cuff V Curwen T Down R Durbin E Eyras J Gilbert M Hammond T Hubbard A Kasprzyk D Keefe H Lehvaslaiho V Iyer C Melsopp E Mongin R Pettett S Potter A Rust E Schmidt S Searle G Slater J Smith W Spooner A Stabenau J Stalker E Stupka A Ureta-Vidal I Vastrik E Birney (2003) ArticleTitleEnsembl 2002: Accommodating comparative genomics Nucleic Acids Res 31 38–42 Occurrence Handle10.1093/nar/gkg083 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSgu7o%3D Occurrence Handle12519943

    Article  CAS  PubMed  Google Scholar 

  • AG Clark S Glanowski R Nielsen PD Thomas A Kejariwal MA Todd DM Tanenbaum D Civello F Lu B Murphy S Ferriera G Wang X Zheng TJ White JJ Sninsky MD Adams M Cargill (2003) ArticleTitleInferring nonneutral evolution from human-chimp-mouse orthologous gene trios Science 302 1960–1963 Occurrence Handle10.1126/science.1088821 Occurrence Handle1:CAS:528:DC%2BD3sXps1ams7Y%3D Occurrence Handle14671302

    Article  CAS  PubMed  Google Scholar 

  • P Dehal P Predki AS Olsen A Kobayashi P Folta S Lucas M Land A Terry CL Ecale Zhou S Rash Q Zhang L Gordon J Kim C Elkin MJ Pollard P Richardson D Rokhsar E Uberbacher T Hawkins E Branscomb L Stubbs (2001) ArticleTitleHuman chromosome 19 and related regions in mouse: conservative and lineage-specific evolution Science 293 104–111 Occurrence Handle10.1126/science.1060310 Occurrence Handle1:CAS:528:DC%2BD3MXltFCntbw%3D Occurrence Handle11441184

    Article  CAS  PubMed  Google Scholar 

  • I Ebersberger D Metzler C Schwarz S Pääbo (2002) ArticleTitleGenomewide comparison of DNA sequences between humans and chimpanzees Am J Hum Genet 70 1490–1497 Occurrence Handle10.1086/340787 Occurrence Handle1:CAS:528:DC%2BD38Xkt1SqsL4%3D Occurrence Handle11992255

    Article  CAS  PubMed  Google Scholar 

  • EE Eichler SM Hoffman AA Adamson LA Gordon P McCready JE Lamerdin HW Mohrenweiser (1998) ArticleTitleComplex β-satellite repeat structures and the expansion of the zinc finger gene cluster in 19p12 Genome Res 8 791–808 Occurrence Handle1:CAS:528:DyaK1cXlvFaitLk%3D Occurrence Handle9724325

    CAS  PubMed  Google Scholar 

  • J Felsenstein (1993) PHYLIP (phylogeny inference package). Version 3.5c. Distributed by the author Department of Genetics, University of Washington, Seattle .

    Google Scholar 

  • N Galtier D Mouchiroud (1998) ArticleTitleIsochore evolution in mammals: A human-like ancestral structure Genetics 150 1577–1584 Occurrence Handle1:CAS:528:DyaK1MXitVelug%3D%3D Occurrence Handle9832533

    CAS  PubMed  Google Scholar 

  • G Glusman I Yanai I Rubin D Lancet (2001) ArticleTitleThe complete human olfactory subgenome Genome Res 11 685–702 Occurrence Handle10.1101/gr.171001 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wmur4%3D Occurrence Handle11337468

    Article  CAS  PubMed  Google Scholar 

  • MJ Greenacre (1984) Theory and applications of correspondence analysis Academic Press London

    Google Scholar 

  • RC Hardison KM Roskin S Yang M Diekhans WJ Kent R Weber L Elnitski J Li M O’Connor D Kolbe S Schwartz TS Furey S Whelan N Goldman A Smit W Miller F Chiaromonte D Haussler (2003) ArticleTitleCovariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution Genome Res 13 13–26 Occurrence Handle10.1101/gr.844103 Occurrence Handle1:CAS:528:DC%2BD3sXnvFGmsg%3D%3D Occurrence Handle12529302

    Article  CAS  PubMed  Google Scholar 

  • M Hasegawa H Kishino T Yano (1985) ArticleTitleDating of the human-ape splitting by a molecular clock of mitochondrial DNA J Mol Evol 22 160–174 Occurrence Handle1:CAS:528:DyaL2MXmtFSns7g%3D Occurrence Handle3934395

    CAS  PubMed  Google Scholar 

  • LD Hurst A Eyre-Walker (2000) ArticleTitleEvolutionary genomics: Reading the bands Bioessays 22 105–107 Occurrence Handle10.1002/(SICI)1521-1878(200002)22:2<105::AID-BIES1>3.0.CO;2-S Occurrence Handle1:CAS:528:DC%2BD3MXmslShtrg%3D Occurrence Handle10655029

    Article  CAS  PubMed  Google Scholar 

  • DT Jones WR Taylor JM Thornton (1992) ArticleTitleThe rapid generation of mutation data matrices from protein sequences Comput Appl Biosci 8 275–282 Occurrence Handle1:CAS:528:DyaK38Xlt1Okt7w%3D Occurrence Handle1633570

    CAS  PubMed  Google Scholar 

  • 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) ArticleTitleThe UCSC Genome Browser Database Nucleic Acids Res. 31 51–54 Occurrence Handle10.1093/nar/gkg129 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSgu7g%3D Occurrence Handle12519945

    Article  CAS  PubMed  Google Scholar 

  • ES Lander et al. (2001) ArticleTitleInitial sequencing and analysis of the human genome Nature 409 860–921 Occurrence Handle10.1038/35057062 Occurrence Handle11237011

    Article  PubMed  Google Scholar 

  • MJ Lercher EJ Williams LD Hurst (2001) ArticleTitleLocal similarity in evolutionary rates extends over whole chromosomes in human-rodent and mouse-rat comparisons: implications for understanding the mechanistic basis of the male mutation bias Mol Biol Evol 18 2032–2039 Occurrence Handle1:CAS:528:DC%2BD3MXotVSlsbw%3D Occurrence Handle11606699

    CAS  PubMed  Google Scholar 

  • MJ Lercher AO Urrutia LD Hurst (2002) ArticleTitleClustering of housekeeping genes provides a unified model of gene order in the human genome Nat Genet 31 180–183 Occurrence Handle10.1038/ng887 Occurrence Handle1:CAS:528:DC%2BD38XktVKgtrw%3D Occurrence Handle11992122

    Article  CAS  PubMed  Google Scholar 

  • WH Li S Yi K Makova (2002) ArticleTitleMale-driven evolution Curr Opin Genet Dev 12 650–656 Occurrence Handle10.1016/S0959-437X(02)00354-4 Occurrence Handle1:CAS:528:DC%2BD38XosFOhsrg%3D Occurrence Handle12433577

    Article  CAS  PubMed  Google Scholar 

  • C Looman M Abrink C Mark L Hellman (2002) ArticleTitleKRAB zinc finger proteins: An analysis of the molecular mechanisms governing their increase in numbers and complexity during evolution Mol Biol Evol 19 2118–2130 Occurrence Handle1:CAS:528:DC%2BD38Xps12hs7w%3D Occurrence Handle12446804

    CAS  PubMed  Google Scholar 

  • G Matassi PM Sharp C Gautier (1999) ArticleTitleChromosomal location effects on gene sequence evolution in mammals Curr Biol 9 786–791 Occurrence Handle10.1016/S0960-9822(99)80361-3 Occurrence Handle1:CAS:528:DyaK1MXltFChur4%3D Occurrence Handle10469563

    Article  CAS  PubMed  Google Scholar 

  • NJ Mulder R Apweiler TK Attwood A Bairoch D Barrell A Bateman D Binns M Biswas P Bradley P Bork P Bucher RR Copley E Courcelle U Das R Durbin L Falquet W Fleischmann S Griffiths-Jones D Haft N Harte N Hulo D Kahn A Kanapin M Krestyaninova R Lopez I Letunic D Lonsdale V Silventoinen SE Orchard M Pagni D Peyruc CP Ponting JD Selengut F Servant CJ Sigrist R Vaughan EM Zdobnov (2003) ArticleTitleThe InterPro Database, 2003 brings increased coverage and new features Nucleic Acids Res 31 315–318 Occurrence Handle10.1093/nar/gkg046 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSmsbo%3D Occurrence Handle12520011

    Article  CAS  PubMed  Google Scholar 

  • SB Needleman CD Wunsch (1970) ArticleTitleA general method applicable to the search for similarities in the amino acid sequence of two proteins J Mol Biol 48 443–453 Occurrence Handle1:CAS:528:DyaE3cXktVShu74%3D Occurrence Handle5420325

    CAS  PubMed  Google Scholar 

  • KD Pruitt DR Maglott (2001) ArticleTitleRefSeq and LocusLink: NCBI gene-centered resources Nucleic Acids Res 29 137–140 Occurrence Handle10.1093/nar/29.1.137 Occurrence Handle1:CAS:528:DC%2BD3MXjtlWnu74%3D Occurrence Handle11125071

    Article  CAS  PubMed  Google Scholar 

  • S Saccone C Federico G Bernardi (2002) ArticleTitleLocalization of the gene-richest and the gene-poorest isochores in the interphase nuclei of mammals and birds Gene 300 169–178 Occurrence Handle10.1016/S0378-1119(02)01038-7 Occurrence Handle1:CAS:528:DC%2BD38XptFaksb8%3D Occurrence Handle12468098

    Article  CAS  PubMed  Google Scholar 

  • M Shannon AT Hamilton L Gordon E Branscomb L Stubbs (2003) ArticleTitleDifferential expansion of zinc-finger transcription factor loci in homologous human and mouse gene clusters Genome Res 13 1097–1110 Occurrence Handle10.1101/gr.963903 Occurrence Handle1:CAS:528:DC%2BD3sXksFehu7k%3D Occurrence Handle12743021

    Article  CAS  PubMed  Google Scholar 

  • J Smith IR Paton F Murray RP Crooijmans MA Groenen DW Burt (2002a) ArticleTitleComparative mapping of human chromosome 19 with the chicken shows conserved synteny and gives an insight into chromosomal evolution Mamm Genome 13 310–315 Occurrence Handle10.1007/s00335-001-3071-1 Occurrence Handle1:CAS:528:DC%2BD38Xlt1Cht7s%3D

    Article  CAS  Google Scholar 

  • NG Smith MT Webster H Ellegren (2002b) ArticleTitleDeterministic mutation rate variation in the human genome Genome Res 12 1350–1356 Occurrence Handle10.1101/gr.220502 Occurrence Handle1:CAS:528:DC%2BD38Xnt1elsbo%3D

    Article  CAS  Google Scholar 

  • DL Swofford (1998) PAUP*: Phylogenetic analysis using parsimony (*and other methods) Version 4. Sinauer Associates Sunderland

    Google Scholar 

  • H Tanabe S Muller M Neusser J Hase Particlevon E Calcagno M Cremer I Solovei C Cremer T Cremer (2002) ArticleTitleEvolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates Proc Natl Acad Sci USA 99 4424–4429 Occurrence Handle10.1073/pnas.072618599 Occurrence Handle1:CAS:528:DC%2BD38XivFShtLs%3D Occurrence Handle11930003

    Article  CAS  PubMed  Google Scholar 

  • The Gene Ontology Consortium (2001) ArticleTitleCreating the gene ontology resource: Design and implementation Genome Res 11 1425–1433 Occurrence Handle10.1101/gr.180801 Occurrence Handle11483584

    Article  PubMed  Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • JC, Venter et al. (2001) ArticleTitleThe sequence of the human genome Science 291 1304–1351 Occurrence Handle10.1126/science.1058040 Occurrence Handle1:CAS:528:DC%2BD3MXhtlSgsbo%3D Occurrence Handle11181995

    Article  CAS  PubMed  Google Scholar 

  • AE Vinogradov (2003) ArticleTitleDNA helix: The importance of being GC-rich Nucleic Acids Res 31 1838–1844 Occurrence Handle10.1093/nar/gkg296 Occurrence Handle1:CAS:528:DC%2BD3sXisFequrs%3D Occurrence Handle12654999

    Article  CAS  PubMed  Google Scholar 

  • RH, Waterston et al. (2002) ArticleTitleInitial sequencing and comparative analysis of the mouse genome Nature 420 520–562 Occurrence Handle10.1038/nature01262 Occurrence Handle12466850

    Article  PubMed  Google Scholar 

  • KH Wolfe PM Sharp WH Li (1989) ArticleTitleMutation rates differ among regions of the mammalian genome Nature 337 283–285 Occurrence Handle10.1038/337283a0 Occurrence Handle1:STN:280:BiaD1MjivVU%3D Occurrence Handle2911369

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

J.C. and M.A. are recipients of a Ramón y Cajal contract of the Spanish Ministerio de Ciencia y Tecnología (MCYT) and are supported by grant numbers BIO2002-04426-C02-02 and BIO2002-04426-C02-01, respectively, from the Plan Nacional de Investigación Científica, Desarrollo e Innovación Tecnológica (I+D+I) of the MCYT, cofinanced with FEDER funds. We thank Alison Shaw, Xavier Estivill, Arcadi Navarro, and Martin Lercher for carefully reading the manuscript and making useful suggestions.

Author information

Authors and Affiliations

  1. Centre de Regulació Genòmica (CRG), Programme of Bioinformatics and Genomics, Passeig Marítim 37-49, 08003, Barcelona, Spain

    Jose Castresana & Roderic Guigó

  2. Grup de Recerca en Informàtica Biomèdica, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Passeig Marítim 37-49, 08003, Barcelona, Spain

    Roderic Guigó & M. Mar Albà

Authors
  1. Jose Castresana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roderic Guigó
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Mar Albà
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jose Castresana.

Additional information

Department of Physiology and Molecular Biodiversity, Institut de Biologia Molecular de Barcelona, CSIC, Jordi Girona 18, 08034 Barcelona, Spain

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castresana, J., Guigó, R. & Albà, M.M. Clustering of Genes Coding for DNA Binding Proteins in a Regionof Atypical Evolution of the Human Genome. J Mol Evol 59, 72–79 (2004). https://doi.org/10.1007/s00239-004-2605-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-2605-z

Keywords

Search

Navigation