Genetic Properties Influencing the Evolvability of Gene Expression

• DOI: 10.1126/science.1140247
• Publication Date: 2007-05-25T01:05:50Z
• Authors: Christian R. Landry; Bernardo Lemos; Scott A. Rifkin; W. J. Dickinson; Daniel L. Hartl
• Keywords: 0303 health sciences; Binding Sites; Models, Genetic; Transcription, Genetic; Genes, Fungal; Gene Expression; Genetic Variation; Saccharomyces cerevisiae; TATA Box; Evolution, Molecular; 03 medical and health sciences; Phenotype; Gene Expression Regulation, Fungal; Mutation; Linear Models; Gene Regulatory Networks; Selection, Genetic; Promoter Regions, Genetic; Oligonucleotide Array Sequence Analysis; Transcription Factors

Identifying the properties of gene networks that influence their evolution is a fundamental research goal. However, modes of evolution cannot be inferred solely from the distribution of natural variation, because selection interacts with demography and mutation rates to shape polymorphism and divergence. We estimated the effects of naturally occurring mutations on gene expression while minimizing the effect of natural selection. We demonstrate that sensitivity of gene expression to mutations increases with both increasing trans-mutational target size and the presence of a TATA box. Genes with greater sensitivity to mutations are also more sensitive to systematic environmental perturbations and stochastic noise. These results provide a mechanistic basis for gene expression evolvability that can serve as a foundation for realistic models of regulatory evolution.