Gene duplication and the evolution of ribosomal protein gene regulation in yeast
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Wapinski-2010-Gene duplication and.pdf
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Author(s)
Regev, Aviv
Wapinski, Ilan
Pfiffner, Jenna
French, Courtney
Socha, Amanda
Thompson, Dawn Anne
Date Issued
March 2010
Journal
Proceedings of the National Academy of Sciences of the United States of America. (PNAS)
Publisher
National Academy of Sciences (U.S.)
Citation
Wapinski, I. et al. “Gene duplication and the evolution of ribosomal protein gene regulation in yeast.” Proceedings of the National Academy of Sciences 107.12 (2010): 5505-5510. Copyright ©2011 by the National Academy of Sciences
Version
Final published version
Abstract
Coexpression of genes within a functional module can be conserved at great evolutionary distances, whereas the associated regulatory mechanisms can substantially diverge. For example, ribosomal protein (RP) genes are tightly coexpressed in Saccharomyces cerevisiae, but the cis and trans factors associated with them are surprisingly diverged across Ascomycota fungi. Little is known, however, about the functional impact of such changes on actual expression levels or about the selective pressures that affect them. Here, we address this question in the context of the evolution of the regulation of RP gene expression by using a comparative genomics approach together with cross-species functional assays. We show that an activator (Ifh1) and a repressor (Crf1) that control RP gene regulation in normal and stress conditions in S. cerevisiae are derived from the duplication and subsequent specialization of a single ancestral protein. We provide evidence that this regulatory innovation coincides with the duplication of RP genes in a whole-genome duplication (WGD) event and may have been important for tighter control of higher levels of RP transcripts. We find that subsequent loss of the derived repressor led to the loss of a stress-dependent repression of RPs in the fungal pathogen Candida glabrata. Our comparative computational and experimental approach shows how gene duplication can constrain and drive regulatory evolution and provides a general strategy for reconstructing the evolutionary trajectory of gene regulation across species.
MIT Department
Massachusetts Institute of Technology. Department of Biology
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DOI of Published Version
https://doi.org/10.1073/pnas.0911905107
