GSE192880
Recent Cis-Trans Coevolution Driven by the Emergence of A Novel Gene in Drosophila
Young, or newly evolved, genes arise ubiquitously across the tree of life, and can rapidly acquire novel functions that influence a diverse array of biological processes (Chen et al. 2013)1.  Previous work identified a young regulatory gene in Drosophila, Zeus, which diverged rapidly from its parent Caf40 and took on roles in the male reproductive system.  This neofunctionalization was accompanied by differential binding of the Zeus protein to loci throughout the Drosophila melanogaster genome Chen et al. 2012)2.  However, the way in which new DNA-binding proteins acquire and co-evolve with their targets in the genome is not understood. Here, by comparing Zeus ChIP-seq data from D. melanogaster and D. simulans to the ancestral Caf40 binding events from D. yakuba, a species that diverged before the duplication event, we find a dynamic pattern in which Zeus binding rapidly co-evolved with a previously unknown DNA motif under the influence of positive selection.  Interestingly, while both copies of Zeus acquired targets at male-biased and testis-specific genes, D. melanogaster and D. simulans proteins have specialized binding on different chromosomes, a pattern echoed in the evolution of the associated motif.  Our results suggest that evolution of young regulatory genes can be coupled to substantial re-wiring of the transcriptional networks into which they integrate, even over short evolutionary timescales.  Our results thus uncover dynamic, genome-wide evolutionary processes associated with new genes. Overall design: Generation of Transgenic Drosophila Lines: Expression vectors were constructed for each gene of interest and were transformed into white-eyed D. melanogaster. Briefly, each coding sequence (Dmel Zeus, Dsim Zeus, and Dyak Caf40) was cloned so as to be linked to an Actin5C promoter and FLAG tag, and then inserted into the piggyBac MWpBacFPNS vector (Bloomington Drosophila Genomics Resource Center, Stock Number 1289). Transformations of D. melanogaster were performed by Rainbow Transgenics, Inc. (Camarillo, CA) ChIP-seq Data Production:  ChIP-seq experiments were performed using standard modEncode protocols after collecting adults in each species. Four (4) technical replicates were performed for each transgenic Drosophila line. Sequencing data was generated by the High-Throughput Genome Analysis Core (HGAC) at the Institute for Genomics and Systems Biology, University of Chicago