Effects of mutation and selection on plasticity of a promoter activity in Saccharomyces cerevisiae

Abstract

Phenotypic plasticity is an evolvable property of biological systems that can arise from environment-specific regulation of gene expression. To better understand the evolutionary and molecular mechanisms that give rise to plasticity in gene expression, we quantified the effects of 235 single-nucleotide mutations in the promoter ( ) on the activity of this promoter in media containing glucose, galactose, or glycerol as a carbon source. We found that the distributions of mutational effects differed among environments because many mutations altered the plastic response exhibited by the wild-type allele. Comparing the effects of these mutations with the effects of 30 polymorphisms on expression plasticity in the same environments provided evidence of natural selection acting to prevent the plastic response in activity between glucose and galactose from becoming larger. The largest changes in expression plasticity were observed between fermentable (glucose or galactose) and nonfermentable (glycerol) carbon sources and were caused by mutations located in the RAP1 and GCR1 transcription factor binding sites. Mutations altered expression plasticity most frequently between the two fermentable environments, with mutations causing significant changes in plasticity between glucose and galactose distributed throughout the promoter, suggesting they might affect chromatin structure. Taken together, these results provide insight into the molecular mechanisms underlying gene-by-environment interactions affecting gene expression as well as the evolutionary dynamics affecting natural variation in plasticity of gene expression.

Fitness effects of altering gene expression noise inSaccharomyces cerevisiae

“…Assuming that the average expression level of a population is near the fitness optimum in a stable environment, but further from the optimum following a change in the environment, our results unify studies showing that increasing expression noise tends to be deleterious in a constant environment but beneficial in a fluctuating one (Fraser et al 2004;Blake et al 2006;Batada and Hurst 2007;Lehner 2008;Tǎnase-Nicola and Ten Wolde 2008;Zhang et al 2009;Fraser and Kaern 2009;Ito et al 2009;Wang and Zhang 2011;Levy et al 2012;Wolf et al 2015;Liu et al 2015;Keren et al 2016). Expression noise may be particularly important in the early phase of adaptation to a fluctuating environment, when a new expression optimum makes an increase in noise beneficial and before expression plasticity evolves as a more optimal strategy (Wolf et al 2015;Duveau, Yuan, et al 2017). Perhaps most interestingly, these data show that high levels of noise can transition from being deleterious to beneficial even in a stable environment following a change in average expression level to a level further from the fitness optimum.…”

Fitness effects of altering gene expression noise in Saccharomyces cerevisiae

“…Expression noise may be particularly important in the early phase of adaptation to a fluctuating environment, when a new expression optimum makes an increase in noise beneficial and before expression plasticity evolves as a more optimal strategy ( Wolf et al, 2015 ). Such plasticity in expression level seems to have already evolved for TDH3 ( Duveau et al, 2017b ). Our data suggest that high levels of expression noise can also be beneficial in a stable environment when the mean expression level is far from optimal.…”

Regulation plays a multifaceted role in the retention of gene duplicates

“…This observation suggests that responsiveness could be a gene property that favors divergence between species. However, this is not a universal trend, as responsiveness could also be selected against for many genes that would rather require stable dosage [16].…”