Cell Reports (Sep 2015)

Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers

  • Zeba Wunderlich,
  • Meghan D.J. Bragdon,
  • Ben J. Vincent,
  • Jonathan A. White,
  • Javier Estrada,
  • Angela H. DePace

DOI
https://doi.org/10.1016/j.celrep.2015.08.021
Journal volume & issue
Vol. 12, no. 11
pp. 1740 – 1747

Abstract

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Many developmental genes are controlled by shadow enhancers—pairs of enhancers that drive overlapping expression patterns. We hypothesized that compensatory evolution can maintain the total expression of a gene, while individual shadow enhancers diverge between species. To test this hypothesis, we analyzed expression driven by orthologous pairs of shadow enhancers from Drosophila melanogaster, Drosophila yakuba, and Drosophila pseudoobscura that control expression of Krüppel, a transcription factor that patterns the anterior-posterior axis of blastoderm embryos. We found that the expression driven by the pair of enhancers is conserved between these three species, but expression levels driven by the individual enhancers are not. Using sequence analysis and experimental perturbation, we show that each shadow enhancer is regulated by different transcription factors. These results support the hypothesis that compensatory evolution can occur between shadow enhancers, which has implications for mechanistic and evolutionary studies of gene regulation.