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Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Drosophila Species

Johnson, WC and Ordway, AJ and Watada, M and Pruitt, JN and Williams, TM and Rebeiz, M (2015) Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Drosophila Species. PLoS Genetics, 11 (6). ISSN 1553-7390

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Abstract

© 2015 Johnson et al. The modification of transcriptional regulation has become increasingly appreciated as a major contributor to morphological evolution. However, the role of negative-acting control elements (e.g. silencers) in generating morphological diversity has been generally overlooked relative to positive-acting “enhancer” elements. The highly variable body coloration patterns among Drosophilid insects represents a powerful model system in which the molecular alterations that underlie phenotypic diversity can be defined. In a survey of pigment phenotypes among geographically disparate Japanese populations of Drosophila auraria, we discovered a remarkable degree of variation in male-specific abdominal coloration. In testing the expression patterns of the major pigment-producing enzymes, we found that phenotypes uniquely correlated with differences in the expression of ebony, a gene required for yellow-colored cuticle. Assays of ebony’s transcriptional control region indicated that a lightly pigmented strain harbored cis-regulatory mutations that caused correlated changes in its expression. Through a series of chimeric reporter constructs between light and dark strain alleles, we localized function-altering mutations to a conserved silencer that mediates a male-specific pattern of ebony repression. This suggests that the light allele was derived through the loss of this silencer’s activity. Furthermore, examination of the ebony gene of D. serrata, a close relative of D. auraria which secondarily lost male-specific pigmentation revealed the parallel loss of this silencer element. These results demonstrate how loss-of-function mutations in a silencer element resulted in increased gene expression. We propose that the mutational inactivation of silencer elements may represent a favored path to evolve gene expression, impacting morphological traits.


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Details

Item Type: Article
Status: Published
Creators/Authors:
CreatorsEmailPitt UsernameORCID
Johnson, WC
Ordway, AJ
Watada, M
Pruitt, JN
Williams, TM
Rebeiz, Mrebeiz@pitt.eduREBEIZ0000-0001-5731-5570
Contributors:
ContributionContributors NameEmailPitt UsernameORCID
EditorDesplan, ClaudeUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Date: 1 January 2015
Date Type: Publication
Access Restriction: No restriction; Release the ETD for access worldwide immediately.
Journal or Publication Title: PLoS Genetics
Volume: 11
Number: 6
DOI or Unique Handle: 10.1371/journal.pgen.1005279
Institution: University of Pittsburgh
Schools and Programs: Dietrich School of Arts and Sciences > Biological Sciences
Refereed: Yes
ISSN: 1553-7390
Date Deposited: 23 Aug 2016 13:40
Last Modified: 05 Feb 2019 11:55
URI: http://d-scholarship.pitt.edu/id/eprint/28522

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