1. Department of Biochemistry & Biophysics,
2. Department of Microbiology & Immunology, University of California San Francisco, San Francisco, California 94143-2200, USA
3. †Present address: Department of Molecular and Cell Biology, University of California Berkeley, Lawrence Berkeley National Labs, 1 Cyclotron Road, Mailstop 84-355, Berkeley, California 94703, USA
4. *These authors contributed equally to this work

Correspondence to: Alexander D. Johnson^1,2 Microarray data are available in Supplementary Information and at http://genome.ucsf.edu/asg_evolution/. Correspondence and requests for materials should be addressed to A.D.J. (Email: ajohnson@cgl.ucsf.edu).

Abstract

Evolution of gene regulation is an important contributor to the variety of life. Here, we analyse the evolution of a combinatorial transcriptional circuit composed of sequence-specific DNA-binding proteins that are conserved among all eukaryotes. This circuit regulates mating in the ascomycete yeast lineage. We first identify a group of mating genes that was transcriptionally regulated by an activator in a fungal ancestor, but is now transcriptionally regulated by a repressor in modern bakers' yeast. Despite this change in regulatory mechanism, the logical output of the overall circuit remains the same. By examining the regulation of mating in modern yeasts that are related to different extents, we deduce specific, sequential changes in both cis- and trans-regulatory elements that constitute the transition from positive to negative regulation. These changes indicate specific mechanisms by which fitness barriers were traversed during the transition.

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