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
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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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    ABSTRACT: How populations that inhabit the same geographical area become genetically differentiated is not clear. To investigate this, we characterized phenotypic and genetic differences between two populations of Saccharomyces cerevisiae that in some cases inhabit the same environment but show relatively little gene flow. We profiled stress sensitivity in a group of vineyard isolates and a group of oak-soil strains and found several niche-related phenotypes that distinguish the populations. We performed bulk-segregant mapping on two of the distinguishing traits: the vineyard-specific ability to grow in grape juice and oak-specific tolerance to the cell wall damaging drug Congo red. To implicate causal genes, we also performed a chemical genomic screen in the lab-strain deletion collection and identified many important genes that fell under QTL peaks. One gene important for growth in grape juice and identified by both the mapping and the screen was SSU1, a sulfite-nitrite pump implicated in wine fermentations. The beneficial allele is generated by a known translocation that we reasoned may also serve as a genetic barrier. We found that the translocation is prevalent in vineyard strains, but absent in oak strains, and presents a post-zygotic barrier to spore viability. Furthermore, the translocation was associated with a fitness cost to the rapid growth rate seen in oak-soil strains. Our results reveal the translocation as a dual-function locus that enforces ecological differentiation while producing a genetic barrier to gene flow in these sympatric populations. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Molecular Biology and Evolution 05/2015; 32(9). DOI:10.1093/molbev/msv112 · 9.11 Impact Factor
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    • "This set of rapidly-diverging genes is characterized by a so-called Occupied Proximal Nucleosome promoter structure that lacks a defined nucleosome-free region and displays a TATA binding site [14], [15]. In addition, functionally related genes tend to change in a coordinated manner, both when compared across environments and when compared between related strains or species [12], [16], most likely reflecting the abundance of trans-mutations affecting environmentally-sensitive regulators [15]. "
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    ABSTRACT: Cells adapt to environmental changes through genetic mutations that stabilize novel phenotypes. Often, this adaptation involves regulatory changes which modulate gene expression. In the budding yeast, ribosomal-related gene expression correlates with cell growth rate across different environments. To examine whether the same relationship between gene expression and growth rate is observed also across natural populations, we measured gene expression, growth rate and ethanol production of twenty-four wild type yeast strains originating from diverse habitats, grown on the pentose sugar xylulose. We found that expression of ribosome-related genes did not correlate with growth rate. Rather, growth rate was correlated with the expression of amino acid biosynthesis genes. Searching other databases, we observed a similar correlation between growth rate and amino-acid biosyntehsis genes in a library of gene deletions. We discuss the implications of our results for understanding how cells coordinate their translation capacity with available nutrient resources.
    PLoS ONE 02/2014; 9(2):e88801. DOI:10.1371/journal.pone.0088801 · 3.23 Impact Factor
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    • "Taken together, our findings provide a case in which the rare and often deleterious mutations that litter wild yeast genomes (Zorgo et al. 2012) follow a compelling evolutionary logic. A broader involvement of additional metals is suggested by the growth defect of a Malaysian isolate in high-copper medium (Hodgins-Davis et al. 2012). The emerging picture is one in which the Malaysian yeast population has experienced unique evolutionary pressures on metal metabolism, highlighting the palm flower niche of these microbes as a driver of evolutionary change. "
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    ABSTRACT: Comparative-genomic studies have reported widespread variation in levels of gene expression within and between species. Using these data to infer organism-level trait divergence has proven to be a key challenge in the field. We have used a wild Malaysian population of Saccharomyces cerevisiae as a testbed in the search to predict and validate trait differences based on observations of regulatory variation. Malaysian yeast, when cultured in standard medium, activated regulatory programs that protect cells from the toxic effects of high iron. Malaysian yeast also showed a hyperactive regulatory response during culture in the presence of excess iron, and had a unique growth defect in high-iron conditions. Molecular validation experiments pinpointed the iron metabolism factors AFT1, CCC1, and YAP5 as contributors to these molecular and cellular phenotypes, and in genome-scale sequence analyses, a suite of iron-toxicity response genes showed evidence for rapid protein evolution in Malaysian yeast. Our findings support a model in which iron metabolism has diverged in Malaysian yeast as a consequence of a change in selective pressure, with Malaysian alleles shifting the dynamic range of iron response to low iron concentrations and weakening resistance to extreme iron toxicity. By dissecting the iron-scarcity specialist behavior of Malaysian yeast, our work highlights the power of expression divergence as a signpost for biologically and evolutionarily relevant variation at the organismal level.
    G3-Genes Genomes Genetics 10/2013; 3(12). DOI:10.1534/g3.113.008011 · 3.20 Impact Factor
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