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The gain and loss of functional transcription factor binding sites has been proposed as a major source of evolutionary change in  cis- regulatory DNA and gene expression. We have developed an evolutionary model to study binding-site turnover that uses multiple sequence alignments to assess the evolutionary constraint on individual binding sites, and to map gain and loss events along a phylogenetic tree. We apply this model to study the evolutionary dynamics of binding sites of the  Drosophila melanogaster  transcription factor Zeste, using genome-wide in vivo (ChIP–chip) binding data to identify functional Zeste binding sites, and the genome sequences of  D. melanogaster ,  D. simulans ,  D. erecta,  and  D. yakuba  to study their evolution. We estimate that more than 5% of functional Zeste binding sites in  D. melanogaster  were gained along the  D. melanogaster  lineage or lost along one of the other lineages. We find that Zeste-bound regions have a reduced rate of binding-site loss and an increased rate of binding-site gain relative to flanking sequences. Finally, we show that binding-site gains and losses are asymmetrically distributed with respect to  D. melanogaster , consistent with lineage-specific acquisition and loss of Zeste-responsive regulatory elements.

Large-Scale Turnover of Functional Transcription Factor Binding Sites in Drosophila