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

1 , 1 , 1 , 2 , *

PLoS Genetics

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      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.

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      Most cited references 90

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      The fly Drosophila melanogaster is one of the most intensively studied organisms in biology and serves as a model system for the investigation of many developmental and cellular processes common to higher eukaryotes, including humans. We have determined the nucleotide sequence of nearly all of the approximately 120-megabase euchromatic portion of the Drosophila genome using a whole-genome shotgun sequencing strategy supported by extensive clone-based sequence and a high-quality bacterial artificial chromosome physical map. Efforts are under way to close the remaining gaps; however, the sequence is of sufficient accuracy and contiguity to be declared substantially complete and to support an initial analysis of genome structure and preliminary gene annotation and interpretation. The genome encodes approximately 13,600 genes, somewhat fewer than the smaller Caenorhabditis elegans genome, but with comparable functional diversity.
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        Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology.

        Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
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          Mobile elements: drivers of genome evolution.

          Mobile elements within genomes have driven genome evolution in diverse ways. Particularly in plants and mammals, retrotransposons have accumulated to constitute a large fraction of the genome and have shaped both genes and the entire genome. Although the host can often control their numbers, massive expansions of retrotransposons have been tolerated during evolution. Now mobile elements are becoming useful tools for learning more about genome evolution and gene function.
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            Author and article information

            Affiliations
            [1 ]Department of Organismal Biology and Anatomy, The College, The University of Chicago, Chicago, Illinois, United States of America
            [2 ]The Committees on Evolutionary Biology, Genetics, and Molecular Medicine, The College, The University of Chicago, Chicago, Illinois, United States of America
            Fred Hutchinson Cancer Research Center, United States of America
            Author notes
            * To whom correspondence should be addressed. E-mail: m-feder@ 123456uchicago.edu
            Contributors
            Role: Editor
            Journal
            PLoS Genet
            pgen
            PLoS Genetics
            Public Library of Science (San Francisco, USA )
            1553-7390
            1553-7404
            October 2006
            6 October 2006
            17 August 2006
            : 2
            : 10
            1592238
            10.1371/journal.pgen.0020165
            06-PLGE-RA-0200R2 plge-02-10-04
            17029562
            (Editor)
            Copyright: © 2006 Walser et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
            Counts
            Pages: 15
            Categories
            Research Article
            Ecology
            Evolution
            Molecular Biology - Structural Biology
            Physiology
            Drosophila
            Custom metadata
            Walser JC, Chen B, Feder ME (2006) Heat-shock promoters: Targets for evolution by P transposable elements in Drosophila. PLoS Genet 2(10): e165. DOI: 10.1371/journal.pgen.0020165

            Genetics

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