Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers

Cell Reports
Zeba WunderlichAngela H DePace

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.

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Citations

Apr 26, 2018·Wiley Interdisciplinary Reviews. Systems Biology and Medicine·Julia M Rogers, Martha L Bulyk
Oct 5, 2017·Proceedings of the National Academy of Sciences of the United States of America·Xin ZhuEzzat El-Sherif
Mar 18, 2016·PloS One·Javier EstradaAngela H DePace
Jan 31, 2018·Nature Ecology & Evolution·Charles G DankoAdam Siepel
May 3, 2019·G3 : Genes - Genomes - Genetics·Zeba WunderlichAngela H DePace
Nov 16, 2019·PLoS Computational Biology·Kenneth BarrOvidiu Radulescu
Apr 4, 2020·PLoS Genetics·Duo XuEkta Khurana
Sep 4, 2020·Genetics·Stephen Small, David N Arnosti
Jan 15, 2021·Nature Reviews. Genetics·Evgeny Z KvonZeba Wunderlich
Dec 4, 2019·Journal of Theoretical Biology·Clémence Réda, Bartek Wilczyński
Jul 1, 2019·G3 : Genes - Genomes - Genetics·Zeba WunderlichAngela H DePace
May 7, 2021·Genetics·Stephen Small, David N Arnosti
Jul 3, 2021·Insects·Hasiba Asma, Marc S Halfon
Sep 28, 2021·IScience·Rachel WaymackZeba Wunderlich

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