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Does Positive Selection Drive Transcription Factor Binding Site
Turnover? A Test with Drosophila Cis-Regulatory Modules


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.


Vyšlo v časopise: Does Positive Selection Drive Transcription Factor Binding Site Turnover? A Test with Drosophila Cis-Regulatory Modules. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002053
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002053

Souhrn

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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Štítky
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