Coordinated Genome-Wide Modifications within Proximal Promoter Cis-regulatory Elements during Vertebrate Evolution

There often exists a “one-to-many” relationship between a transcription factor and a multitude of binding sites throughout the genome. It is commonly assumed that transcription factor binding motifs remain largely static over the course of evolution because changes in binding specificity can alter the interactions with potentially hundreds of sites across the genome. Focusing on regulatory motifs overrepresented at specific locations within or near the promoter, we find that a surprisingly large number of cis-regulatory elements have been subject to coordinated genome-wide modifications during vertebrate evolution, such that the motif frequency changes on a single branch of vertebrate phylogeny. This was found to be the case even between closely related mammal species, with nearly a third of all location-specific consensus motifs exhibiting significant modifications within the human or mouse lineage since their divergence. Many of these modifications are likely to be compensatory changes throughout the genome following changes in protein factor binding affinities, whereas others may be due to changes in mutation rates or effective population size. The likelihood that this happened many times during vertebrate evolution highlights the need to examine additional taxa and to understand the evolutionary and molecular mechanisms underlying the evolution of protein–DNA interactions.

[1]  Takashi Gojobori,et al.  Genome Biology and Evolution , 2010, Genome Biology and Evolution.

[2]  Hao Li,et al.  Evolution of Transcription Networks — Lessons from Yeasts , 2010, Current Biology.

[3]  Guy Baele,et al.  Modelling the ancestral sequence distribution and model frequencies in context-dependent models for primate non-coding sequences , 2010, BMC Evolutionary Biology.

[4]  Katja Nowick,et al.  Lineage-specific transcription factors and the evolution of gene regulatory networks. , 2010, Briefings in functional genomics.

[5]  K. Verstrepen,et al.  Promoter architecture and the evolvability of gene expression , 2009, Journal of biology.

[6]  A. Lane,et al.  Structural analysis of the DNA target site and its interaction with Mbp1. , 2009, Organic & biomolecular chemistry.

[7]  Robert S Illingworth,et al.  CpG islands – ‘A rough guide’ , 2009, FEBS letters.

[8]  Uwe Ohler,et al.  Measuring spatial preferences at fine-scale resolution identifies known and novel cis-regulatory element candidates and functional motif-pair relationships , 2009, Nucleic acids research.

[9]  Esther T. Chan,et al.  Conservation of core gene expression in vertebrate tissues , 2009, Journal of biology.

[10]  Justin C. Fay,et al.  Correction: Frequent Gain and Loss of Functional Transcription Factor Binding Sites , 2009, PLoS Computational Biology.

[11]  Alfonso Valencia,et al.  Progress and challenges in predicting protein-protein interaction sites , 2008, Briefings Bioinform..

[12]  Günter P. Wagner,et al.  The Origin of Conserved Protein Domains and Amino Acid Repeats Via Adaptive Competition for Control Over Amino Acid Residues , 2009, Journal of Molecular Evolution.

[13]  Guy Baele,et al.  A model-based approach to study nearest-neighbor influences reveals complex substitution patterns in non-coding sequences. , 2008, Systematic biology.

[14]  Venky N. Iyer,et al.  Sepsid even-skipped Enhancers Are Functionally Conserved in Drosophila Despite Lack of Sequence Conservation , 2008, PLoS genetics.

[15]  J. T. Kadonaga,et al.  The RNA polymerase II core promoter - the gateway to transcription. , 2008, Current opinion in cell biology.

[16]  Olivier Bodenreider,et al.  The biological function of some human transcription factor binding motifs varies with position relative to the transcription start site , 2008, Nucleic acids research.

[17]  D. W. Knowles,et al.  Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm , 2008, PLoS biology.

[18]  Daniel J. Blankenberg,et al.  28-way vertebrate alignment and conservation track in the UCSC Genome Browser. , 2007, Genome research.

[19]  Zhiping Weng,et al.  Analysis of overrepresented motifs in human core promoters reveals dual regulatory roles of YY1. , 2007, Genome research.

[20]  Bronwen L. Aken,et al.  Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences , 2007, Nature.

[21]  Panayiotis V. Benos,et al.  STAMP: a web tool for exploring DNA-binding motif similarities , 2007, Nucleic Acids Res..

[22]  S. Hannenhalli,et al.  Position and distance specificity are important determinants of cis-regulatory motifs in addition to evolutionary conservation , 2007, Nucleic acids research.

[23]  Scott Doniger,et al.  Frequent Gain and Loss of Functional Transcription Factor Binding Sites , 2007, PLoS Comput. Biol..

[24]  Eugene Bolotin,et al.  Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters. , 2007, Gene.

[25]  G. Wray.  The evolutionary significance of cis-regulatory mutations , 2007, Nature Reviews Genetics.

[26]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[27]  Jun Kawai,et al.  Evolutionary turnover of mammalian transcription start sites. , 2006, Genome research.

[28]  Laurie Gordon,et al.  A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. , 2006, Genome research.

[29]  K. Lindblad-Toh,et al.  Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals , 2005, Nature.

[30]  C. Vinson,et al.  Clustering of DNA sequences in human promoters. , 2004, Genome research.

[31]  Bonnie Berger,et al.  Methods in Comparative Genomics: Genome Correspondence, Gene Identification and Regulatory Motif Discovery , 2004, J. Comput. Biol..

[32]  Johannes Berg,et al.  Adaptive evolution of transcription factor binding sites , 2003, BMC Evolutionary Biology.

[33]  Terrence S. Furey,et al.  The UCSC Table Browser data retrieval tool , 2004, Nucleic Acids Res..

[34]  Matthew W. Hahn,et al.  The evolution of transcriptional regulation in eukaryotes. , 2003, Molecular biology and evolution.

[35]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[36]  Nigel Thrift,et al.  A Rough Guide , 2003 .

[37]  Alexander E. Kel,et al.  TRANSFAC®: transcriptional regulation, from patterns to profiles , 2003, Nucleic Acids Res..

[38]  Janet M Thornton,et al.  Protein-DNA interactions: amino acid conservation and the effects of mutations on binding specificity. , 2002, Journal of molecular biology.

[39]  Mouse Genome Sequencing Consortium.  Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[40]  T. Eulgem.  Eukaryotic transcription factors , 2001, Genome Biology.

[41]  Akif Uzman,et al.  Molecular Cell Biology (4th edition): Harvey Lodish, Arnold Berk, S. Lawrence Zipursky, Paul Matsudaira, David Baltimore and James Darnell; Freeman & Co., New York, NY, 2000, 1084 pp., list price $102.25, ISBN 0-7167-3136-3 , 2001 .

[42]  Donna R. Maglott,et al.  RefSeq and LocusLink: NCBI gene-centered resources , 2001, Nucleic Acids Res..

[43]  International Human Genome Sequencing Consortium.  Initial sequencing and analysis of the human genome , 2001, Nature.

[44]  Donna R. Maglott,et al.  NCBI's LocusLink and RefSeq , 2000, Nucleic Acids Res..

[45]  A. Aggarwal,et al.  Structure of the even‐skipped homeodomain complexed to AT‐rich DNA: new perspectives on homeodomain specificity. , 1995, The EMBO journal.

[46]  R. Roeder,et al.  TATA‐binding protein‐associated factor(s) in TFIID function through the initiator to direct basal transcription from a TATA‐less class II promoter. , 1994, The EMBO journal.

[47]  G. Yarrington.  Molecular Cell Biology , 1987, The Yale Journal of Biology and Medicine.