Polygenic evolution of a sugar specialization trade-off in yeast

• Published in: Nature (London) 2016-02, Vol.530 (7590), p.336-339
• Main Authors: Roop, Jeremy I., Chang, Kyu Chul, Brem, Rachel B.
• Format: Article
• Language: English
• Subjects: 631/181/2474; 631/181/735; 631/208/182; 631/208/199; Adaptation (Biology); Alleles; Analysis; Carbohydrate Metabolism - drug effects; Carbohydrate Metabolism - genetics; Conserved Sequence - genetics; Culture Media - chemistry; Culture Media - pharmacology; Enzymes; Evolution, Molecular; Evolutionary genetics; Galactose; Galactose - metabolism; Gene expression; Gene Expression Regulation, Fungal; Genes, Fungal - genetics; Genetic aspects; Genetic Fitness - genetics; Genetic Loci - genetics; Genetic recombination; Genetics; Genotype & phenotype; Glucose; Glucose - metabolism; Growth rate; Humanities and Social Sciences; Influence; letter; Metabolism; multidisciplinary; Multifactorial Inheritance - genetics; Phenotype; Phylogeny; Promoter Regions, Genetic - genetics; Saccharomyces - classification; Saccharomyces - drug effects; Saccharomyces - genetics; Saccharomyces - metabolism; Saccharomyces cerevisiae - drug effects; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism; Science; Yeast; Yeasts
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature16938

An evolutionary trade-off of unprecedented genetic complexity in the glucose/galactose utilization regulatory pathway across several long-diverged species of Saccharomyces . Keeping track of evolutionary change The evolutionary genetics involved in the development of a single phenotypic trait can be complex, involving many different genes and long tracts of time. Here Rachel Brem and colleagues dissect the changes in the glucose/galactose utilization regulatory pathway across several yeast species that have allowed for the evolution of sugar specialization. They identify a suite of divergent loci mediating a fitness trade-off between reproductively isolated species. This work suggests that that genetic mapping of complex phenotypes is a realistic goal, even in deeply diverged species. The evolution of novel traits can involve many mutations scattered throughout the genome 1 , 2 . Detecting and validating such a suite of alleles, particularly if they arose long ago, remains a key challenge in evolutionary genetics 1 , 2 , 3 . Here we dissect an evolutionary trade-off of unprecedented genetic complexity between long-diverged species. When cultured in 1% glucose medium supplemented with galactose, Saccharomyces cerevisiae , but not S. bayanus or other Saccharomyces species, delayed commitment to galactose metabolism until glucose was exhausted. Promoters of seven galactose ( GAL ) metabolic genes from S. cerevisiae , when introduced together into S. bayanus , largely recapitulated the delay phenotype in 1% glucose–galactose medium, and most had partial effects when tested in isolation. Variation in GAL coding regions also contributed to the delay when tested individually in 1% glucose–galactose medium. When combined, S. cerevisiae GAL coding regions gave rise to profound growth defects in the S. bayanus background. In medium containing 2.5% glucose supplemented with galactose, wild-type S. cerevisiae repressed GAL gene expression and had a robust growth advantage relative to S. bayanus ; transgenesis of S. cerevisiae GAL promoter alleles or GAL coding regions was sufficient for partial reconstruction of these phenotypes. S. cerevisiae GAL genes thus encode a regulatory program of slow induction and avid repression, and a fitness detriment during the glucose–galactose transition but a benefit when glucose is in excess. Together, these results make clear that genetic mapping of complex phenotypes is within reach, even in deeply diverged species.