Polygenic evolution of a sugar specialization tradeoff 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
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature16938

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 - 3 . Here we dissect an evolutionary tradeoff 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.