Heat-shock promoters: targets for evolution by P transposable elements in Drosophila.
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.
Walser
Jean-Claude
JC
Department of Organismal Biology and Anatomy, The College, The University of Chicago, Chicago, Illinois, United States of America.
Chen
Bing
B
Feder
Martin E
ME
D000818:Animals; D004252:DNA Mutational Analysis; D004251:DNA Transposable Elements / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D005787:Gene Frequency; D017344:Genes, Insect; D005843:Geography; D006360:Heat-Shock Proteins / Q000235:genetics*; D016254:Mutagenesis, Insertional; D011401:Promoter Regions, Genetic / Q000235:genetics*; D011995:Recombination, Genetic
D004251:DNA Transposable Elements; D006360:Heat-Shock Proteins