Abstract
Because there is considerable variation in gene expression even between closely related species, it is clear that gene regulatory mechanisms evolve relatively rapidly. Because primary sequence conservation is an unreliable proxy for functional conservation of cis-regulatory elements, their assessment must be carried out in vivo. We conducted a survey of cis-regulatory conservation between C. elegans and closely related species C. briggsae, C. remanei, C. brenneri, and C. japonica. We tested enhancers of eight genes from these species by introducing them into C. elegans and analyzing the expression patterns they drove. Our results support several notable conclusions. Most exogenous cis elements direct expression in the same cells as their C. elegans orthologs, confirming gross conservation of regulatory mechanisms. However, the majority of exogenous elements, when placed in C. elegans, also directed expression in cells outside endogenous patterns, suggesting functional divergence. Recurrent ectopic expression of different promoters in the same C. elegans cells may reflect biases in the directions in which expression patterns can evolve due to shared regulatory logic of coexpressed genes. The fact that, despite differences between individual genes, several patterns repeatedly emerged from our survey, encourages us to think that general rules governing regulatory evolution may exist and be discoverable.
Highlights
A complex network of molecular interactions that orchestrates gene expression provides multiple sources for regulatory variation between species [1]
Gene regulation is a complex biochemical process and it is not a priori clear whether general trends even exist. We systematically addressed this question by testing, in C. elegans, the functions of regulatory elements of eight different genes from four other nematodes
While the differences were usually seen in a relatively small number of cells, there was a discernible trend – there were many more instances of gain, rather than loss of expression, compared to patterns directed by the C. elegans cis elements
Summary
A complex network of molecular interactions that orchestrates gene expression provides multiple sources for regulatory variation between species [1]. Changes in transcriptional regulation can occur in two fundamentally different ways: in trans regulators [2,3], for example through changes in protein sequences or expression patterns of transcription factors, or in cis elements via changes in identity or location of transcription factor binding sites [4,5]. Our research has focused on cis-regulatory elements (CREs). These sequences consist of multiple transcription factor binding sites and a core promoter, but these motifs tend to be short, diffuse, and flexible in their locations [12]. Because cis elements integrate signals from multiple trans-acting factors in the context of an intact cell, their functions have to be assessed in vivo [14]
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