title: Differential paralog divergence modulates genome evolution across yeast species.
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 sulfate 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.
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.|Molecular and Cellular Biology Program, University of Washington, Seattle, Washington, United States of America.
authors.forename: Monica R
authors.identifier: 0000-0003-4413-9058
authors.initials: MR
authors.lastname: Sanchez
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Aaron W
authors.identifier: 0000-0001-5037-9539
authors.initials: AW
authors.lastname: Miller
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Ivan
authors.identifier: 0000-0001-6972-6705
authors.initials: I
authors.lastname: Liachko
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Anna B
authors.identifier: 0000-0003-2456-6626
authors.initials: AB
authors.lastname: Sunshine
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Bryony
authors.initials: B
authors.lastname: Lynch
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Mei
authors.initials: M
authors.lastname: Huang
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Erica
authors.initials: E
authors.lastname: Alcantara
authors.affiliation: Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America.
authors.forename: Christopher G
authors.initials: CG
authors.lastname: DeSevo
authors.affiliation: Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America.
authors.forename: Dave A
authors.initials: DA
authors.lastname: Pai
authors.affiliation: Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America.
authors.forename: Cheryl M
authors.identifier: 0000-0003-2967-7448
authors.initials: CM
authors.lastname: Tucker
authors.affiliation: Howard Hughes Medical Institute and Department of Embryology, Carnegie Institution, Baltimore, Maryland, United States of America.|Department of Biology, Johns Hopkins University, Baltimore, Maryland, United States of America.
authors.forename: Margaret L
authors.initials: ML
authors.lastname: Hoang
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: Maitreya J
authors.identifier: 0000-0001-9944-2666
authors.initials: MJ
authors.lastname: Dunham
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D027321:Anion Transport Proteins / Q000235:genetics*; D019143:Evolution, Molecular; D056084:Genetic Fitness; D014644:Genetic Variation; D016681:Genome, Fungal; D005838:Genotype; D009154:Mutation; D012441:Saccharomyces cerevisiae / Q000235:genetics; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics*; D012641:Selection, Genetic; D000076988:Sulfate Transporters
chemical_list: D027321:Anion Transport Proteins; C094656:SUL1 protein, S cerevisiae; C105781:SUL2 protein, S cerevisiae; D029701:Saccharomyces cerevisiae Proteins; D000076988:Sulfate Transporters