Dataset Information

Gene duplication and the evolution of ribosomal protein gene regulation in yeast.

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.

SUBMITTER: Wapinski I

PROVIDER: S-EPMC2851827 | biostudies-other | 2010 Mar

REPOSITORIES: biostudies-other

ACCESS DATA

Publications

Gene duplication and the evolution of ribosomal protein gene regulation in yeast.

Wapinski Ilan I Pfiffner Jenna J French Courtney C Socha Amanda A Thompson Dawn Anne DA Regev Aviv A

Proceedings of the National Academy of Sciences of the United States of America 20100308 12

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 t ...[more]

PMID: 20212107

Similar Datasets

Project description:BackgroundGene duplication has been a fundamental process in the evolution of eukaryotic genomes. After duplication one copy (or both) can undergo divergence in sequence, expression pattern, and function. Two divergent copies of the ribosomal protein S13 gene (rps13) of chloroplast origin are found in the nucleus of the rosids Arabidopsis, Gossypium, and Glycine. One encodes chloroplast-imported RPS13 (nucp rps13), while the other encodes mitochondria-imported RPS13 (numit rps13). The rps13 gene has been lost from mitochondrial DNA (mt rps13) of many rosids.ResultsWe studied sequence evolution of numit rps13 in comparison with nucp rps13 in seven rosid genera. Ka/Ks analysis and likelihood ratio tests showed considerably higher Ka values and Ka/Ks ratios in numit rps13 than in nucp rps13, indicating increased amino acid sequence divergence in numit rps13. Two positively selected codons were detected in numit RPS13 in regions that are inferred to interact with the 16S rRNA. Several amino acids in numit RPS13 have changed from the one present in nucp RPS13 to the one present in mt RPS13, showing that numit rps13 is becoming more like mt rps13. Comparison of expression patterns and levels of numit rps13 and nucp rps13 in Arabidopsis using microarray data indicated divergence in gene expression. We discovered that in addition to numit rps13, Malus (apple) contains a transcribed mt rps13 gene. To determine if partitioning of expression takes place between numit rps13 and mt rps13, expression of both copies and RNA editing of mt rps13 were examined by RT-PCR, qRT-PCR, and sequencing from 14 different organ types plus seedlings subjected to five different abiotic stresses. Co-expression of numit rps13 and mt rps13 was observed in all the organs and various stress treatments. We determined that purifying selection is acting on both numit rps13 and mt rps13 in Malus.ConclusionOur data provide evidence that numit rps13 genes in rosids have experienced adaptive sequence evolution and convergent evolution with mt rps13. Co-expression of numit rps13 and mt rps13 and purifying selection on both genes in Malus suggest that both are functional. The three organellar rps13 genes in rosids provide a distinctive case of gene duplication involving the co-evolution of the nuclear and cytoplasmic genomes.

Project description:BackgroundConvergent and parallel evolution provide unique insights into the mechanisms of natural selection. Some of the most striking convergent and parallel (collectively recurrent) amino acid substitutions in proteins are adaptive, but there are also many that are selectively neutral. Accordingly, genome-wide assessment has shown that recurrent sequence evolution in orthologs is chiefly explained by nearly neutral evolution. For paralogs, more frequent functional change is expected because additional copies are generally not retained if they do not acquire their own niche. Yet, it is unknown to what extent recurrent sequence differentiation is discernible after independent gene duplications in different eukaryotic taxa.ResultsWe develop a framework that detects patterns of recurrent sequence evolution in duplicated genes. This is used to analyze the genomes of 90 diverse eukaryotes. We find a remarkable number of families with a potentially predictable functional differentiation following gene duplication. In some protein families, more than ten independent duplications show a similar sequence-level differentiation between paralogs. Based on further analysis, the sequence divergence is found to be generally asymmetric. Moreover, about 6% of the recurrent sequence evolution between paralog pairs can be attributed to recurrent differentiation of subcellular localization. Finally, we reveal the specific recurrent patterns for the gene families Hint1/Hint2, Sco1/Sco2 and vma11/vma3.ConclusionsThe presented methodology provides a means to study the biochemical underpinning of functional differentiation between paralogs. For instance, two abundantly repeated substitutions are identified between independently derived Sco1 and Sco2 paralogs. Such identified substitutions allow direct experimental testing of the biological role of these residues for the repeated functional differentiation. We also uncover a diverse set of families with recurrent sequence evolution and reveal trends in the functional and evolutionary trajectories of this hitherto understudied phenomenon.

Dataset Information

Gene duplication and the evolution of ribosomal protein gene regulation in yeast.

Publications

Gene duplication and the evolution of ribosomal protein gene regulation in yeast.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets