Reduced Translational Efficiency of Eukaryotic Genes after Duplication Events

• Published in: Molecular biology and evolution Vol. 37; no. 5; pp. 1452 - 1461
• Main Authors: Chang, Andrew Ying-Fei, Liao, Ben-Yang
• Format: Journal Article
• Language: English
• Published: United States Oxford University Press 01.05.2020
• Subjects: Animals; Biological Evolution; Caenorhabditis elegans; Gene Duplication; Protein Biosynthesis; Proteome; Saccharomyces cerevisiae; Schizosaccharomyces; Transcriptome; protein synthesis; translatome; nematode; stoichiometric imbalance; dosage sensitivity; fungi
• ISSN: 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msz309

Abstract Control of gene expression has been found to be predominantly determined at the level of protein translation. However, to date, reduced expression from duplicated genes in eukaryotes for dosage maintenance has only been linked to transcriptional control involving epigenetic mechanisms. Here, we hypothesize that dosage maintenance following gene duplication also involves regulation at the protein level. To test this hypothesis, we compared transcriptome and proteome data of yeast models, Saccharomyces cerevisiae and Schizosaccharomyces pombe, and worm models, Caenorhabditis elegans and Caenorhabditis briggsae, to investigate lineage-specifically duplicated genes. Duplicated genes in both eukaryotic models exhibited a reduced protein-to-mRNA abundance ratio. Moreover, dosage sensitive genes, represented by genes encoding protein complex subunits, reduced their protein-to-mRNA abundance ratios more significantly than the other genes after duplication events. An analysis of ribosome profiling (Ribo-Seq) data further showed that reduced translational efficiency was more prominent for dosage sensitive genes than for the other genes. Meanwhile, no difference in protein degradation rate was associated with duplication events. Translationally repressed duplicated genes were also more likely to be inhibited at the level of transcription. Taken together, these results suggest that translation-mediated dosage control is partially contributed by natural selection and it enhances transcriptional control in maintaining gene dosage after gene duplication events during eukaryotic genome evolution.