Differential paralog divergence modulates genome evolution across yeast species

Autor: Mei Huang, Ivan Liachko, Monica R. Sanchez, Maitreya J. Dunham, Erica Alcantara, Aaron W. Miller, Margaret L. Hoang, Dave A. Pai, Cheryl M. Tucker, Anna B. Sunshine, Bryony Lynch, Christopher G. DeSevo
Rok vydání: 2017
Předmět:
Evolutionary Genetics
0301 basic medicine
Cancer Research
Genetic Fitness
Yeast and Fungal Models
Paradoxus
Fungal Evolution
Genome Evolution
Genetics (clinical)
2. Zero hunger
Genetics
Experimental evolution
Sulfates
Genomics
Adaptation
Physiological

Chemistry
Experimental Organism Systems
Sulfate Transporters
Physical Sciences
Genome
Fungal

Research Article
Genome evolution
Saccharomyces cerevisiae Proteins
Genotype
lcsh:QH426-470
Anion Transport Proteins
Saccharomyces cerevisiae
Locus (genetics)
Mycology
Biology
Research and Analysis Methods
Molecular Evolution
Evolution
Molecular

Saccharomyces
03 medical and health sciences
Model Organisms
Selection
Genetic

Molecular Biology
Ecology
Evolution
Behavior and Systematics

Comparative genomics
Evolutionary Biology
Human evolutionary genetics
Organisms
Fungi
Gene Amplification
Chemical Compounds
Biology and Life Sciences
Computational Biology
Genetic Variation
Comparative Genomics
biology.organism_classification
Yeast
lcsh:Genetics
030104 developmental biology
Genetic Loci
Evolutionary biology
Mutation
Salts
Zdroj: PLoS Genetics, Vol 13, Iss 2, p e1006585 (2017)
PLoS Genetics
ISSN: 1553-7404
Popis: 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.
Author summary Both comparative genomics and experimental evolution are powerful tools that can be used to make inferences about evolutionary processes. Together, these approaches provide the opportunity to observe evolutionary adaptation over millions of years where selective history is largely unknown, and over short timescales under controlled selective pressures in the laboratory. We have used comparative experimental evolution to observe the evolutionary fate of an adaptive mutation, and determined to what degree the outcome is conditional on the genetic background. We evolved several populations of different yeast species for over 200 generations in sulfate-limited conditions to determine how the differences in genomic context can alter evolutionary routes when challenged with a nutrient limitation selection pressure. We find that the gene encoding a high affinity sulfur transporter becomes amplified in most species of Saccharomyces, except in S. uvarum, in which the amplification of the paralogous sulfate transporter gene SUL2 is recovered. We attribute this change in amplification preference to mutations in the non-coding region of SUL1, likely due to reduced expression of this gene in S. uvarum. We conclude that the adaptive mutations selected for in each organism depend on the genomic context, even when faced with the same environmental condition.
Databáze: OpenAIRE