Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules

Bin Z He; Alisha K Holloway; Sebastian J Maerkl; Martin Kreitman

doi:10.1371/journal.pgen.1002053

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Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules

Journal article

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Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules

Bin Z He, Alisha K Holloway, Sebastian J Maerkl and Martin Kreitman

PLoS genetics, Vol.7(4), pp.e1002053-e1002053

04/2011

DOI: 10.1371/journal.pgen.1002053

PMCID: PMC3084208

PMID: 21572512

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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.

Protein Binding - genetics

Species Specificity

Gene Expression Regulation

Selection, Genetic

Databases, Genetic

Binding Sites - genetics

Phylogeny

Transcription Factors - genetics

Drosophila Proteins - metabolism

Drosophila melanogaster - genetics

Sequence Analysis, DNA

Polymorphism, Genetic

Biological Evolution

Drosophila melanogaster - metabolism

Transcription Factors - metabolism

Animals

Models, Genetic

Drosophila - metabolism

Drosophila Proteins - genetics

Mutation

Drosophila - genetics

Details

Title: Subtitle: Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules
Creators: Bin Z He - Department of Ecology and Evolution, The University of Chicago, Chicago, Illinois, USA. hebin@uchicago.edu
Alisha K Holloway
Sebastian J Maerkl
Martin Kreitman
Resource Type: Journal article
Publication Details: PLoS genetics, Vol.7(4), pp.e1002053-e1002053
DOI: 10.1371/journal.pgen.1002053
PMID: 21572512
PMCID: PMC3084208
NLM abbreviation: PLoS Genet
ISSN: 1553-7390
eISSN: 1553-7404
Publisher: United States
Grant note: R01 GM078381 / NIGMS NIH HHS\nGM078381 / NIGMS NIH HHS
Language: English
Date published: 04/2011
Academic Unit: Biology
Record Identifier: 9983991960702771

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