Academic journal article Genetics

Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila Melanogaster

Academic journal article Genetics

Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila Melanogaster

Article excerpt

ABSTRACT

The packaging of DNA into proper chromatin structure contributes to transcriptional regulation. This packaging is environment sensitive, yet its role in adaptation to novel environmental conditions is completely unknown. We set out to identify candidate chromatin-remodeling loci that are differentiated between tropical and temperate populations in Drosophila melanogaster, an ancestrally equatorial African species that has recently colonized temperate environments around the world. Here we describe sequence variation at seven such chromatin-remodeling loci, four of which (chd1, ssrp, chm, and glu) exhibit strong differentiation between tropical and temperate populations. An in-depth analysis of chm revealed sequence differentiation restricted to a small portion of the gene, as well as evidence of clinal variation along the east coasts of both the United States and Australia. The functions of chd1, chm, ssrp, and glu point to several novel hypotheses for the role of chromatin-based transcriptional regulation in adaptation to a novel environment. Specifically, both stress-induced transcription and developmental homeostasis emerge as potential functional targets of environment-dependent selection.

THE level, timing, and spatial distribution of gene expression vary both within and between species (Oleksiak et al. 2002; Meiklejohn et al. 2003; Rifkin et al. 2003; Nuzhdin et al. 2004; Gilad et al. 2006). Recent work on the evolution of gene expression has focused largely on local regulatory elements (cis-regulation; Gompel et al. 2005; Wittkopp 2006) or on the expression/activity of proteins that interact with such sequences (trans-regulation; Wittkopp et al. 2004; Wang et al. 2007). These DNA-transcription factor interactions, however, compose only one component of gene regulation. The packaging of DNA into proper chromatin structure provides an additional level of transcriptional regulation (Elgin and Workman 2001). For example, variation in chromatin state (i.e., permissive or restrictive) may affect access of cis-regulatory sequence by transcription factors. Recent chromatin research, buttressed by new tools and key insights, is rapidly revealing the complex and elegant mechanisms of chromatin remodeling and their transcriptional consequences (Allis et al. 2007). Evolutionary biologists now have the unprecedented opportunity to explore how this fundamental component of gene regulation contributes to adaptation.

The packaging of DNA into chromatin is environment sensitive. Early Drosophila work demonstrated the temperature sensitivity of two classic chromatin-related phenotypes-position-effect variegation (PEV) (Gowen 1933) and polytene chromosome "puff" induction (Ashburner 1967). More recent studies demonstrate that silencing maintained by the Polycomb group genes (PcGs), which remodel chromatin at developmentally important loci to maintain developmental trajectories (Lewis 1978; Schwartz and Pirrotta 2007), increases with increasing temperature (Fauvarque and Dura 1993). Moreover, stress induces global histone hypoacetylation that results in a coordinated downregulation of transcription (Berthiaume et al. 2006), particularly at components of the translation apparatus (Causton et al. 2001). The promoters of stress response genes, in contrast, experience chromatin remodeling that results in transcriptional activation (yeast: Zhao et al. 2005; Uffenbeck and Krebs 2006; Drosophila: Leibovitch et al. 2002). Finally, stress responders such as heat-shock proteins (which are generalized environmental-response molecules) co-immunoprecipitate with such known chromatin- remodeling complexes as TAC1 (Smith et al. 2004) and the PcG complex, PRC1 (Wang and Brock 2003). Given that chromatin dynamics are environment sensitive, the evolution of proteins that remodel chromatin may contribute to adaptation to novel habitats.

Tolerance of environmental stresses varies both within and between species. The low-latitude species Drosophila virilis, for example, maintains both elevated thermotolerance and an elevated heat-shock protein (hsp) induction threshold relative to the closely related, highlatitude species, D. …

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