Promoter architecture and the evolvability of gene expression

Abstract

Evolutionary changes in gene expression are a main driver of phenotypic evolution. In yeast, genes that have rapidly diverged in expression are associated with particular promoter features, including the presence of a TATA box, a nucleosome-covered promoter and unstable tracts of tandem repeats. Here, we discuss how these promoter properties may confer an inherent capacity for flexibility of expression.

Figure 1

Promoter architecture associated with expression flexibility [46-48]. Top: the architecture of a typical promoter in which nucleosomes are regularly positioned but are excluded from a particular region upstream of the transcription start site. This nucleosome-free region (NFR) contains accessible binding sites for (few) transcriptional regulators (TF). Bottom: the architecture of promoters with high expression flexibility. These promoters tend to have a TATA box and multiple other binding sites for transcriptional regulators. Nucleosome positions are more dynamic (double-headed arrows) and nucleosomes are not strongly excluded from any particular region, and therefore compete with transcriptional regulators at their binding sites. These promoters are thus dependent on the activity of multiple transcriptional regulators and chromatin regulators (CR), which increases their mutational target size.

Figure 2

Expression flexibility, mediated by promoter architecture, may be due to increased dependence on trans regulation and environmental changes. Genes with a TATA box, promoter occupied with nucleosomes and many binding sites are regulated more extensively by regulatory factors. These factors respond to extracellular signals, thus making the target genes responsive to environmental changes both on short timescales (responsiveness and noise) as well as on longer timescales (evolutionary changes). These flexible genes preferentially code for proteins that interact with the environment and mediate the response to environmental changes (curved arrow), and this may allow for rapid adaptation to new environments.