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The extent and nature of epistatic interactions between mutations are issues of fundamental importance in evolutionary biology. However, they are difficult to study and their influence on adaptation remains poorly understood. Here, we use a systems-level approach to examine epistatic interactions that arose during the evolution of  Escherichia coli  in a defined environment. We used expression arrays to compare the effect on global patterns of gene expression of deleting a central regulatory gene,  crp . Effects were measured in two lineages that had independently evolved for 20,000 generations and in their common ancestor. We found that deleting  crp  had a much more dramatic effect on the expression profile of the two evolved lines than on the ancestor. Because the sequence of the  crp  gene was unchanged during evolution, these differences indicate epistatic interactions between  crp  and mutations at other loci that accumulated during evolution. Moreover, a striking degree of parallelism was observed between the two independently evolved lines; 115 genes that were not  crp -dependent in the ancestor became dependent on  crp  in both evolved lines. An analysis of changes in  crp  dependence of well-characterized regulons identified a number of regulatory genes as candidates for harboring beneficial mutations that could account for these parallel expression changes. Mutations within three of these genes have previously been found and shown to contribute to fitness. Overall, these findings indicate that epistasis has been important in the adaptive evolution of these lines, and they provide new insight into the types of genetic changes through which epistasis can evolve. More generally, we demonstrate that expression profiles can be profitably used to investigate epistatic interactions.

Expression Profiles Reveal Parallel Evolution of Epistatic Interactions Involving the CRP Regulon in Escherichia coli