Heat-Shock Promoters: Targets for Evolution by P Transposable Elements in Drosophila

Abstract

Transposable elements are potent agents of genomic change during evolution, but require access to chromatin for insertion—and not all genes provide equivalent access. To test whether the regulatory features of heat-shock genes render their proximal promoters especially susceptible to the insertion of transposable elements in nature, we conducted an unbiased screen of the proximal promoters of 18 heat-shock genes in 48 natural populations of Drosophila. More than 200 distinctive transposable elements had inserted into these promoters; greater than 96% are P elements. By contrast, few or no P element insertions segregate in natural populations in a “negative control” set of proximal promoters lacking the distinctive regulatory features of heat-shock genes. P element transpositions into these same genes during laboratory mutagenesis recapitulate these findings. The natural P element insertions cluster in specific sites in the promoters, with up to eight populations exhibiting P element insertions at the same position; laboratory insertions are into similar sites. By contrast, a “positive control” set of promoters resembling heat-shock promoters in regulatory features harbors few P element insertions in nature, but many insertions after experimental transposition in the laboratory. We conclude that the distinctive regulatory features that typify heat-shock genes (in Drosophila) are especially prone to mutagenesis via P elements in nature. Thus in nature, P elements create significant and distinctive variation in heat-shock genes, upon which evolutionary processes may act.

Synopsis

Transposable elements can be a major source of evolutionary change. Their insertion can directly affect the genes into, or next to, which they insert. To insert, however, they must first gain access to the host gene. The authors reasoned that, because the DNA in the promoters (i.e., regulatory regions) of heat-shock genes is unusually accessible, these genes might harbor many transposable elements. With a technique that can detect any insertion into a gene, they discovered more than 200 distinctive transposable elements in the promoter regions of heat-shock genes in fruit flies from the wild—but few or none in the promoter regions of more typical genes. Surprisingly, out of the one hundred kinds of transposable elements in fruit flies, almost all were P elements. P elements are remarkable because they invaded the fruit fly genome only during the last century. These findings imply that the combination of accessible DNA and the recent invasion of P elements have left a distinctive imprint on the promoters of heat-shock genes.