ArticlePLoS genetics2011
Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules.
Article in PLoS genetics, 2011. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 65 papers.
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Who cites it
65 citing papers in PubMed.
- Cross-species prediction reveals chromatin regions with increased accessibility in humans.Science advances · 2026Article
- Widespread turnover of a conserved cis-regulatory code across 589 grass species.Molecular biology and evolution · 2026Article
- Natural Selection in Transcription Factor-DNA Interaction Motifs: A Comparative and Population Genomics Perspective.Genome biology and evolution · 2025Article
- Experimental approaches to investigate biophysical interactions between homeodomain transcription factors and DNA.Biochimica et biophysica acta. Gene regulatory mechanisms · 2025Review
- Profiling conserved transcription factor binding motifs in Phaseolus vulgaris through comparative genomics.BMC genomics · 2025Article
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- Evolution of transcription factor binding through sequence variations and turnover of binding sites.Genome research · 2022Article
- Article
- Both Binding Strength and Evolutionary Accessibility Affect the Population Frequency of Transcription Factor Binding Sequences in Arabidopsis thaliana.Genome biology and evolution · 2021Article
- Annotating the Insect Regulatory Genome.Insects · 2021Review
- Impact of Genetic Variation in Gene Regulatory Sequences: A Population Genomics Perspective.Frontiers in genetics · 2021Review
- Deep learning suggests that gene expression is encoded in all parts of a co-evolving interacting gene regulatory structure.Nature communications · 2020Article
- REDfly: the transcriptional regulatory element database for Drosophila.Nucleic acids research · 2019Article
- Spatially varying cis-regulatory divergence in Drosophila embryos elucidates cis-regulatory logic.PLoS genetics · 2018Article
- Synthetic enhancer design by in silico compensatory evolution reveals flexibility and constraint in cis-regulation.BMC systems biology · 2017Article
- In silico evolution of the Drosophila gap gene regulatory sequence under elevated mutational pressure.BMC evolutionary biology · 2017Article
- Characterization of dFOXO binding sites upstream of the Insulin Receptor P2 promoter across the Drosophila phylogeny.PloS one · 2017Article
- Translating natural genetic variation to gene expression in a computational model of the Drosophila gap gene regulatory network.PloS one · 2017Article
- Insect antimicrobial peptides act synergistically to inhibit a trypanosome parasite.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2016Article
5 more citing papers are in PubMed but not listed here.
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4 authors.
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Abstract
Transcription factor binding site(s) (TFBS) gain and loss (i.e., turnover) is a well-documented feature of cis-regulatory module (CRM) evolution, yet little attention has been paid to the evolutionary force(s) driving this turnover process. The predominant view, motivated by its widespread occurrence, emphasizes the importance of compensatory mutation and genetic drift. Positive selection, in contrast, although it has been invoked in specific instances of adaptive gene expression evolution, has not been considered as a general alternative to neutral compensatory evolution. In this study we evaluate the two hypotheses by analyzing patterns of single nucleotide polymorphism in the TFBS of well-characterized CRM in two closely related Drosophila species, Drosophila melanogaster and Drosophila simulans. An important feature of the analysis is classification of TFBS mutations according to the direction of their predicted effect on binding affinity, which allows gains and losses to be evaluated independently along the two phylogenetic lineages. The observed patterns of polymorphism and divergence are not compatible with neutral evolution for either class of mutations. Instead, multiple lines of evidence are consistent with contributions of positive selection to TFBS gain and loss as well as purifying selection in its maintenance. In discussion, we propose a model to reconcile the finding of selection driving TFBS turnover with constrained CRM function over long evolutionary time.
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