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

Author(s)

Winslow C. Johnson, University of Pittsburgh
Alison J. Ordway, University of Pittsburgh
Masayoshi Watada, Ehime University
Jonathan N. Pruitt, University of Pittsburgh
Thomas M. Williams, University of DaytonFollow
Mark Rebeiz, University of Pittsburgh

Document Type

Article

Publication Date

6-2015

Publication Source

PLOS Genetics

Abstract

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.

Inclusive pages

1-20

ISBN/ISSN

1553-7390

Document Version

Published Version

Comments

This document is provided for download in compliance with the publisher's open-access policy. Permission documentation is on file.

Copyright

Copyright © 2015, Johnson et al.

Publisher

PLOS

Volume

11

Peer Reviewed

yes

Issue

6

Sponsoring Agency

National Science Foundation, Alfred P. Sloan Foundation, University of Dayton Research Institute, American Heart Association, Howard Hughes Medical Institute Precollege and Undergraduate Science Education Program

eCommons Citation

Johnson, Winslow C.; Ordway, Alison J.; Watada, Masayoshi; Pruitt, Jonathan N.; Williams, Thomas M.; and Rebeiz, Mark, "Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Drosophila Species" (2015). Biology Faculty Publications. 143.
https://ecommons.udayton.edu/bio_fac_pub/143