Maintenance of duplicate genes and their functional redundancy by reduced expression

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA.
Trends in Genetics (Impact Factor: 9.92). 10/2010; 26(10):425-30. DOI: 10.1016/j.tig.2010.07.002
Source: PubMed


Although evolutionary theories predict functional divergence between duplicate genes, many old duplicates still maintain a high degree of functional similarity and are synthetically lethal or sick, an observation that has puzzled many geneticists. We propose that expression reduction, a special type of subfunctionalization, facilitates the retention of duplicates and the conservation of their ancestral functions. Consistent with this hypothesis, gene expression data from both yeasts and mammals show a substantial decrease in the level of gene expression after duplication. Whereas the majority of the expression reductions are likely to be neutral, some are apparently beneficial to rebalancing gene dosage after duplication.

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    • "Redundancy in duplicate genes is difficult to sustain by natural selection (Cooke et al. 1997; Nowak et al. 1997; Wagner 2000; Qian et al. 2010), but ribosomal proteins and histones may be exceptions to this rule due to the requirement for high expression of these types of genes (Kondrashov and Kondrashov 2006; Ihmels et al. 2007; Qian et al. 2010). Such selection on expression magnitude, in combination with selection to maintain dosage balance, would explain the survival of the WGD duplicates for these two classes of genes. "
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    • "Conceivably, the observed trend for paralogs to become more specialized in their expression patterns than expected from the strict DDC model (Table 1) as well as a significant positive correlation between gene expression and sequence divergence for within-species paralog measurements (Figures 1(c) and 1(d)) and the nonmonotonic dependency of the Z-scores and ranking scores on sequence divergence (Figures 1(a) and 1(b)) can be explained by selection for rebalancing of expression in different tissues and environmental conditions (Figure 2) [34]. This scenario, the “protein dosage rebalancing” [34], is consistent with several previous studies which suggest that rebalancing of expression after duplications, at least for some genes, could be beneficial [37–39, 41–44]. For example, Qian and colleagues have shown that yeast and mammalian genes often experienced a significant decrease in the level of expression after duplication. "
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    ABSTRACT: Ongoing debates about functional importance of gene duplications have been recently intensified by a heated discussion of the "ortholog conjecture" (OC). Under the OC, which is central to functional annotation of genomes, orthologous genes are functionally more similar than paralogous genes at the same level of sequence divergence. However, a recent study challenged the OC by reporting a greater functional similarity, in terms of gene ontology (GO) annotations and expression profiles, among within-species paralogs compared to orthologs. These findings were taken to indicate that functional similarity of homologous genes is primarily determined by the cellular context of the genes, rather than evolutionary history. Subsequent studies suggested that the OC appears to be generally valid when applied to mammalian evolution but the complete picture of evolution of gene expression also has to incorporate lineage-specific aspects of paralogy. The observed complexity of gene expression evolution after duplication can be explained through selection for gene dosage effect combined with the duplication-degeneration-complementation model. This paper discusses expression divergence of recent duplications occurring before functional divergence of proteins encoded by duplicate genes.
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