Recurrent Modification of a Conserved Cis-Regulatory Element Underlies Fruit Fly Pigmentation Diversity
| Autor: | David J. Tacy, Eric M. Camino, Joseph R. Salomone, Mark Rebeiz, William A. Rogers, Thomas M. Williams, Kristen A. Davis |
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| Jazyk: | angličtina |
| Rok vydání: | 2013 |
| Předmět: |
Cancer Research
Sex Differentiation lcsh:QH426-470 Regulatory Sequences Nucleic Acid Evolution Molecular 03 medical and health sciences 0302 clinical medicine Genetics Melanogaster Animals Drosophila Proteins Allele Molecular Biology Gene Transcription factor Genetics (clinical) Ecology Evolution Behavior and Systematics Conserved Sequence 030304 developmental biology Homeodomain Proteins 0303 health sciences biology Human evolutionary genetics Pigmentation Gene Expression Regulation Developmental Genetic Variation biology.organism_classification Phenotype Female pigmentation DNA-Binding Proteins lcsh:Genetics Drosophila melanogaster Mutation Female 030217 neurology & neurosurgery Research Article Transcription Factors |
| Zdroj: | PLoS Genetics PLoS Genetics, Vol 9, Iss 8, p e1003740 (2013) |
| ISSN: | 1553-7404 1553-7390 |
| Popis: | The development of morphological traits occurs through the collective action of networks of genes connected at the level of gene expression. As any node in a network may be a target of evolutionary change, the recurrent targeting of the same node would indicate that the path of evolution is biased for the relevant trait and network. Although examples of parallel evolution have implicated recurrent modification of the same gene and cis-regulatory element (CRE), little is known about the mutational and molecular paths of parallel CRE evolution. In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen. Female-specific Bab expression is regulated by the dimorphic element, a CRE that possesses direct inputs from body plan (ABD-B) and sex-determination (DSX) transcription factors. Here, we find that the recurrent evolutionary modification of this CRE underlies both intraspecific and interspecific variation in female pigmentation in the melanogaster species group. By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities. Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages. Collectively, our findings represent an example where the paths of evolution appear biased to a specific CRE, and drastic changes in function were accompanied by deep conservation of key regulatory linkages. Author Summary Trait development occurs through networks of genes that are connected by interactions between transcription factor proteins and binding site sequences within cis-regulatory element (CRE) DNA sequences. These interactions enable CREs to function as switches that control the expression of a gene(s) they regulate. Little is known about the molecular paths by which CREs evolve. Here, we identify a CRE that has repeatedly been the target of mutations that generate diverse pigmentation phenotypes on the abdomen of Drosophila melanogaster and its close relatives. By reconstructing and testing the ancestral form of this enhancer in vivo, we demonstrate that individuals from widely distributed Drosophila melanogaster populations possess modified forms of this CRE. Interestingly, the majority of this divergence proceeded without modifying previously identified binding sites for body plan and sex determination transcription factors. This pattern of extreme functional divergence, with contrasting conservation of transcription factor inputs may reflect strong constraint against modifying regulatory sequences that are required for expression in multiple body regions through shared binding sites. |
| Databáze: | OpenAIRE |
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