Abstract
Genome sequences diverge more rapidly in mammals than in other animal lineages, such as birds or insects. However, the effect of this rapid divergence on transcriptional evolution remains unclear. Recent reports have indicated a faster divergence of transcription factor binding in mammals than in insects, but others found the reverse for mRNA expression. Here, we show that these conflicting interpretations resulted from differing methodologies. We performed an integrated analysis of transcriptional network evolution by examining mRNA expression, transcription factor binding and cis-regulatory motifs across >25 animal species, including mammals, birds and insects. Strikingly, we found that transcriptional networks evolve at a common rate across the three animal lineages. Furthermore, differences in rates of genome divergence were greatly reduced when restricting comparisons to chromatin-accessible sequences. The evolution of transcription is thus decoupled from the global rate of genome sequence evolution, suggesting that a small fraction of the genome regulates transcription.
Highlights
A long-standing question in biology is what fraction of the genome regulates transcription (ENCODE Project Consortium, 2012; Graur et al, 2013; Niu and Jiang, 2013; Kellis et al, 2014)
We considered all GSTFs that were profiled using chromatin immuno-precipitation (ChIP) followed by massively parallel sequencing (ChIPseq) in at least three related species, where separate ChIPs were performed per species
The analyses presented here represent the most comprehensive study conducted to date on the evolution of transcriptional networks across animal lineages
Summary
A long-standing question in biology is what fraction of the genome regulates transcription (ENCODE Project Consortium, 2012; Graur et al, 2013; Niu and Jiang, 2013; Kellis et al, 2014). Recent studies have measured the association between sequence changes and changes in transcript levels, epigenetic modifications or binding of transcription factors regulating specific gene sets (gene-specific transcription factors, GSTF) (Cookson et al, 2009; McVicker et al, 2013; Kasowski et al, 2010; 2013; Heinz et al, 2013; Villar et al, 2014; Wong et al, 2015; Brem et al, 2002; Chan et al, 2009; Shibata et al, 2012) These experiments demonstrated that genomic sequences can influence transcription even in the absence of evolutionary conservation. Such rapid transcriptional evolution would set mammals apart from other metazoans like birds or insects, whose genomes contain far fewer repetitive elements (Taft et al, 2007) and tend to be more constrained (Siepel et al, 2005; Zhang et al, 2014)
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