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Differential paralog divergence modulates evolutionary outcomes in yeast

ABSTRACT: Evolutionary outcomes depend not only on the selective forces acting upon a species, but also on the genetic background. However, large timescales and uncertain historical selection pressures can make it difficult to discern such important background differences between species. Experimental evolution is one tool to compare evolutionary potential of known genotypes in a controlled environment. Here we utilized a highly reproducible evolutionary adaptation in Saccharomyces cerevisiae to investigate whether experimental evolution of other yeast species would select for similar adaptive mutations. We evolved populations of S. cerevisiae, S. paradoxus, S. mikatae, S. uvarum, and interspecific hybrids between S. uvarum and S. cerevisiae for 200-500 generations in sulfate-limited continuous culture. Wild-type S. cerevisiae cultures invariably amplify the high affinity sulfate transporter gene, SUL1. However, while amplification of the SUL1 locus was detected in S. paradoxus and S. mikatae populations, S. uvarum cultures instead selected for amplification of the paralog, SUL2. We measured the relative fitness of strains bearing deletions and amplifications of both SUL genes from different species, confirming that, converse to S. cerevisiae, S. uvarum SUL2 contributes more to fitness in sulfate limitation than S. uvarum SUL1. By measuring the fitness and gene expression of chimeric promoter-ORF constructs, we were able to delineate the cause of this differential fitness effect primarily to the promoter of S. uvarum SUL1. Our data show evidence of differential sub-functionalization among the sulfur transporters across Saccharomyces species through recent changes in noncoding sequence. Furthermore, these results show a clear example of how such background differences due to paralog divergence can drive changes in genome evolution.

ORGANISM(S): Saccharomyces cerevisiae Saccharomyces bayanus

PROVIDER: GSE87401 | GEO | 2016/09/30

SECONDARY ACCESSION(S): PRJNA344847

REPOSITORIES: GEO

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Project description:Chromatin accessibility is an important functional genomics phenotype that influences transcription factor binding and gene expression. Genome-scale technologies allow chromatin accessibility to be mapped with high-resolution, facilitating detailed analyses into the genetic architecture and evolution of chromatin structure within and between species. We performed Formaldehyde-Assisted Isolation of Regulatory Elements sequencing (FAIRE-Seq) to map chromatin accessibility in two parental haploid yeast species, Saccharomyces cerevisiae and Saccharomyces paradoxus and their diploid hybrid. We show that although broad-scale characteristics of the chromatin landscape are well conserved between these species, accessibility is significantly different for 947 regions upstream of genes that are enriched for GO terms such as intracellular transport and protein localization exhibit. We also develop new statistical methods to investigate the genetic architecture of variation in chromatin accessibility between species, and find that cis effects are more common and of greater magnitude than trans effects. Interestingly, we find that cis and trans effects at individual genes are often negatively correlated, suggesting widespread compensatory evolution to stabilize levels of chromatin accessibility. Finally, we demonstrate that the relationship between chromatin accessibility and gene expression levels is complex, and a significant proportion of differences in chromatin accessibility might be functionally benign. There are 20 samples in total. These consist of 10 FAIRE-seq samples, specifically 6 haploid samples, S. cerevisiae strain UWOPS05_217_3 replicates 1 and 2, S. cerevisiae strain DBVPG1373 replicates 1 and 2, and S. paradoxus strain CBS432 replicates 1 and 2. There are also 4 diploid hybrid samples, hybrid between S. cerevisiae strain UWOPS05_217_3 and S. paradoxus strain CBS432 replicates 1 and 2, and the hybrid between S. cerevisiae strain DBVPG1373 and S. paradoxus strain CBS432 replicates 1 and 2. There are also RNA-seq samples for each of these 10 samples.

Project description:A fundamental problem in biology is the molecular basis for divergence among related organisms. We have investigated the level of divergence of transcription factor binding sites for two key factors that regulate developmental processes in the budding yeasts. The genomic binding locations for the Ste12 and Tec1 transcription factors in S. cerevisiae, S. mikatae and S. bayanus were mapped by chromatin immunoprecipitation combined with microarrays (chIP chip)1, 2 and compared to one another. While there was a large core network which was conserved in all three species, there were many instances of binding events whose relative levels differ significantly quantitatively in one species relative to another and as well as species-specific binding events. One interesting class of genes were identified that were bound only in S. mikatae and S. bayanus; many of these genes are targets of Ste12 in haploid strains of S. cerevisiae, suggesting that S. cerevisiae has uniquely acquired the ability to differentially regulate these genes in haploid and diploid cells in these species. To extend these studies, the transcriptional network for the Ste12 homologue (Cph1) in Candida albicans was also mapped and compared to the Saccharomyces species. Again, there were several genes bound by Cph1 which are involved in mating in S. cerevisiae, suggesting that the precise delineation between many mating and pseudohyphal targets by Ste12 may be specific to S. cerevisiae. Overall our results demonstrate that transcription binding sites differ faster than gene content indicating that gene regulation at the level of transcription factor binding is likely to be a major mode of evolutionary divergence between related species. We expect that this divergence is essential for the distinct ecological niches inhabited by these organisms. Keywords: chIP-chip ChIP-chip was performed on Ste12 and Tec1 from S. cerevisiae, S. mikatae and S. bayanus in addition to Cph1 from S. cerevisiae. Three biological replicates were performed for each factor in each species with one replicate representing a dye swap.

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Differential paralog divergence modulates evolutionary outcomes in yeast

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