Dynamic evolution of precise regulatory encodings creates the clustered signature of developmental enhancers

Details Dynamic evolution of precise regulatory encodings creates the clustered signature of developmental enhancers Dynamic evolution of precise regulatory encodings creates the clustered signature of developmental enhancers

2010-04-07

arxiv.org/abs/1004.1028v1

Biology

Quantitative Biology

Populations and Evolution

33 pages, 16 figures, 3 Tables. First presented at the 51st Annual Drosophila Research Conference (DRC), Washington D.C., U.S.

Scientific paper

A morphogenic protein known as Dorsal patterns the embryonic dorsoventral body axis of Drosophila by binding to transcriptional enhancers across the genome. Each such enhancer activates a neighboring gene at a unique threshold concentration of Dorsal. The presence of Dorsal binding site clusters in these enhancers and of similar clusters in other enhancers has motivated models of threshold-encoding in site density. However, we found that the precise length of a spacer separating a pair of specialized Dorsal and Twist binding sites determines the threshold-response. Despite this result, the functional range determined by this spacer element as well as the role and origin of its surrounding Dorsal site cluster remained completely unknown. Here, we experiment with enhancers from diverse Drosophila genomes, including the large uncompacted genomes from ananassae and willistoni, and report three major interdependent results. First, we map the functional range of the threshold-encoding spacer variable. Second, we show that the majority of sites at the cluster are non-functional divergent elements that have been separated beyond the encoding's functional range. Third, we verify an evolutionary model involving the frequent replacement of a threshold encoding, whose precision is easily outdated by shifting accuracy. The process by which encodings are replaced by newer ones is facilitated by the palindromic nature of the Dorsal and Twist binding motifs and by intrinsic repeat-instability in the specialized Twist binding site, which critically impacts the length of the spacer linking it to Dorsal. Over time, the dynamic process of selective deprecation and replacement of encodings adds to a growing cluster of deadened elements, or necro-elements, and strongly biases local sequence composition. ... [ABSTRACT TRUNCATED]

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