Abundant Gene-by-Environment Interactions in Gene Expression Reaction Norms to Copper within Saccharomyces cerevisiae

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT USA 06520.
Genome Biology and Evolution (Impact Factor: 4.23). 09/2012; 4(11). DOI: 10.1093/gbe/evs084
Source: PubMed


Genetic variation for plastic phenotypes potentially contributes phenotypic variation to populations that can be selected during adaptation to novel ecological contexts. However, the basis and extent of plastic variation that manifests in diverse environments remains elusive. Here we characterize copper reaction norms for mRNA abundance among five S. cerevisiae strains to a) describe population variation across the full range of ecologically relevant copper concentrations, from starvation to toxicity, and b) to test the hypothesis that plastic networks exhibit increased population variation for gene expression. We find that although the vast majority of the variation is small in magnitude (considerably less than two-fold), not just some, but most genes demonstrate variable expression across environments, across genetic backgrounds, or both. Plastically expressed genes included both genes regulated directly by copper-binding transcription factors Mac1 and Ace1 and genes indirectly responding to the downstream metabolic consequences of the copper gradient, particularly genes involved in copper, iron, and sulfur homeostasis. Copper-regulated gene networks exhibited more similar behavior within the population in environments where those networks have a large impact on fitness. Nevertheless, expression variation in genes like Cup1, important to surviving copper stress, was linked with variation in mitotic fitness and in the breadth of differential expression across the genome. By revealing a broader and deeper range of population variation, our results provide further evidence for the interconnectedness of genome-wide mRNA levels, their dependence on environmental context and genetic background, and the abundance of variation in gene expression that can contribute to future evolution.

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    • "The distinct lineages partly correlate with geography, environmental niche, and the degree of human association (Fay and Benavides 2005a; Diezmann and Dietrich 2009; Liti et al. 2009; Sicard and Legras 2011; Wang et al. 2012; Hyma and Fay 2013). Phenotypic studies of the species have demonstrated significant variation in phenotypes such as stress tolerance, sporulation efficiency, mRNA and protein levels, and metabolic propensity, some of which vary by lineage and others that are correlated with strain niche (Gerke et al. 2006; Kvitek et al. 2008; Liti et al. 2009; Ehrenreich et al. 2010, 2012; Will et al. 2010; Cubillos et al. 2011; Magwene et al. 2011; Parts et al. 2011; Warringer et al. 2011; Hodgins-Davis et al. 2012; Skelly et al. 2013). Interestingly, some natural populations of S. cerevisiae have been found to co-occur in nature but show only low levels of gene flow (Hyma and Fay 2013). "
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