Rapid Cis–Trans Coevolution Driven by a Novel Gene Retroposed from a Eukaryotic Conserved CCR4–NOT Component in Drosophila

Krinsky, Benjamin H.; Arthur, Robert K.; Xia, Shengqian; Sosa, Dylan; Arsala, Deanna; White, Kevin P.; Long, Manyuan

doi:10.3390/genes13010057

Rapid Cis–Trans Coevolution Driven by a Novel Gene Retroposed from a Eukaryotic Conserved CCR4–NOT Component in Drosophila

Journal Article · Sun Dec 26 00:00:00 EST 2021 · Genes

DOI:https://doi.org/10.3390/genes13010057· OSTI ID:2469941

Krinsky, Benjamin H. ^[1]; Arthur, Robert K. ^[2]; Xia, Shengqian ^[1]; Sosa, Dylan ^[1]; ^[1]; White, Kevin P. ^[2]; Long, Manyuan ^[1]

University of Chicago, IL (United States)
University of Chicago, IL (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)

Young, or newly evolved, genes arise ubiquitously across the tree of life, and they can rapidly acquire novel functions that influence a diverse array of biological processes. Previous work identified a young regulatory duplicate gene in Drosophila, Zeus that unexpectedly diverged rapidly from its parent, Caf40, an extremely conserved component in the CCR4–NOT machinery in post-transcriptional and post-translational regulation of eukaryotic cells, 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. However, the way in which new DNA-binding proteins acquire and coevolve 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 found a dynamic pattern in which Zeus binding rapidly coevolved with a previously unknown DNA motif, which we term Caf40 and Zeus-Associated Motif (CAZAM), 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. Using CRISPR-Cas9-mediated gene knockout of Zeus and RNA-Seq, we found that Zeus regulated the expression of 661 differentially expressed genes (DEGs). Our results suggest that the evolution of young regulatory genes can be coupled to substantial rewiring 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.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: Department of Education GAANN Fellowship; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2469941

Journal Information:: Genes, Journal Name: Genes Journal Issue: 1 Vol. 13; ISSN 2073-4425

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CCR4–NOT
Caf40
ChIP-Seq
DNA motif coevolution
Zeus
cis–trans coevolution
differentially expressed genes (DEGs)
driven force
genetics & heredity
novel gene

Rapid Cis–Trans Coevolution Driven by a Novel Gene Retroposed from a Eukaryotic Conserved CCR4–NOT Component in Drosophila

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