Gene duplication and the evolution of ribosomal protein gene regulation in yeast
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 asso...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2011
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| Online Access: | http://hdl.handle.net/1721.1/61365 https://orcid.org/0000-0001-8567-2049 |
| _version_ | 1826191701107015680 |
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| author | Regev, Aviv Wapinski, Ilan Pfiffner, Jenna French, Courtney Socha, Amanda Thompson, Dawn Anne |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Regev, Aviv Wapinski, Ilan Pfiffner, Jenna French, Courtney Socha, Amanda Thompson, Dawn Anne |
| author_sort | Regev, Aviv |
| collection | MIT |
| description | 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. |
| first_indexed | 2024-09-23T09:00:01Z |
| format | Article |
| id | mit-1721.1/61365 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T09:00:01Z |
| publishDate | 2011 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/613652022-09-26T09:43:44Z Gene duplication and the evolution of ribosomal protein gene regulation in yeast Regev, Aviv Wapinski, Ilan Pfiffner, Jenna French, Courtney Socha, Amanda Thompson, Dawn Anne Massachusetts Institute of Technology. Department of Biology Regev, Aviv Regev, Aviv 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. Alfred P. Sloan Foundation Howard Hughes Medical Institute Burroughs Wellcome Fund National Institutes of Health (U.S.) Broad Institute of MIT and Harvard Human Frontier Science Program (Strasbourg, France) 2011-03-01T23:06:11Z 2011-03-01T23:06:11Z 2010-03 2009-10 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/61365 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 https://orcid.org/0000-0001-8567-2049 en_US http://dx.doi.org/10.1073/pnas.0911905107 Proceedings of the National Academy of Sciences of the United States of America. (PNAS) Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Regev, Aviv Wapinski, Ilan Pfiffner, Jenna French, Courtney Socha, Amanda Thompson, Dawn Anne Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title | Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title_full | Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title_fullStr | Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title_full_unstemmed | Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title_short | Gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| title_sort | gene duplication and the evolution of ribosomal protein gene regulation in yeast |
| url | http://hdl.handle.net/1721.1/61365 https://orcid.org/0000-0001-8567-2049 |
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