Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers

Cell Rep. 2015 Sep 22;12(11):1740-7. doi: 10.1016/j.celrep.2015.08.021. Epub 2015 Sep 3.

Abstract

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / genetics*
  • Drosophila / metabolism*
  • Drosophila Proteins / biosynthesis*
  • Drosophila Proteins / genetics*
  • Enhancer Elements, Genetic*
  • Female
  • Gene Expression Regulation, Developmental
  • Kruppel-Like Transcription Factors / biosynthesis*
  • Kruppel-Like Transcription Factors / genetics*
  • Male

Substances

  • Drosophila Proteins
  • Kr protein, Drosophila
  • Kruppel-Like Transcription Factors