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Complexity of gene expression evolution after duplication: protein dosage rebalancing.

Rogozin IB - Genet Res Int (2014)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.

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.

No MeSH data available.


Related in: MedlinePlus

Schematic representation of the “protein dosage rebalancing” hypothesis [34]. This synthetic model is a combination of the dosage effect and DDC models: many recent gene duplications (or gene copy-number variations (CNVs) at the population level) have a positive effect in some tissues and/or environmental conditions, whereas they also have a negative effect in some other tissues and/or environmental conditions [3, 7, 21–23]. Balancing of positive and negative dosage effects influenced by natural selection may be an important factor which is causing diversification of expression patterns (rebalancing of expression) of duplicate genes in the course of fixation of gene duplications. This process is similar to the conventional dosage effect hypothesis [3]. After the gene duplication is fixed in a population, preservation of this gene duplication may be largely explained by the DDC model (maintenance of duplicate genes due to differential loss or reduction of expression in various tissues).
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fig2: Schematic representation of the “protein dosage rebalancing” hypothesis [34]. This synthetic model is a combination of the dosage effect and DDC models: many recent gene duplications (or gene copy-number variations (CNVs) at the population level) have a positive effect in some tissues and/or environmental conditions, whereas they also have a negative effect in some other tissues and/or environmental conditions [3, 7, 21–23]. Balancing of positive and negative dosage effects influenced by natural selection may be an important factor which is causing diversification of expression patterns (rebalancing of expression) of duplicate genes in the course of fixation of gene duplications. This process is similar to the conventional dosage effect hypothesis [3]. After the gene duplication is fixed in a population, preservation of this gene duplication may be largely explained by the DDC model (maintenance of duplicate genes due to differential loss or reduction of expression in various tissues).

Mentions: Similar observations have been reported previously for paralogous genes in yeast [45] and fly [46]. Oakley and coworkers used a phylogenetic approach to demonstrate that the fast evolutionary rate of tissue-specific repression or loss of gene expression is significantly higher than the rate of activation or gain [46]. It was also found that DDC is consistent with only a portion of possible ancestral histories of gene expression [46]. 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. It was suggested that although the majority of the expression reduction is likely to be neutral, for some of duplicate genes, it could be beneficial through the rebalanced gene dosage [41].


Complexity of gene expression evolution after duplication: protein dosage rebalancing.

Rogozin IB - Genet Res Int (2014)

Schematic representation of the “protein dosage rebalancing” hypothesis [34]. This synthetic model is a combination of the dosage effect and DDC models: many recent gene duplications (or gene copy-number variations (CNVs) at the population level) have a positive effect in some tissues and/or environmental conditions, whereas they also have a negative effect in some other tissues and/or environmental conditions [3, 7, 21–23]. Balancing of positive and negative dosage effects influenced by natural selection may be an important factor which is causing diversification of expression patterns (rebalancing of expression) of duplicate genes in the course of fixation of gene duplications. This process is similar to the conventional dosage effect hypothesis [3]. After the gene duplication is fixed in a population, preservation of this gene duplication may be largely explained by the DDC model (maintenance of duplicate genes due to differential loss or reduction of expression in various tissues).
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4150538&req=5

fig2: Schematic representation of the “protein dosage rebalancing” hypothesis [34]. This synthetic model is a combination of the dosage effect and DDC models: many recent gene duplications (or gene copy-number variations (CNVs) at the population level) have a positive effect in some tissues and/or environmental conditions, whereas they also have a negative effect in some other tissues and/or environmental conditions [3, 7, 21–23]. Balancing of positive and negative dosage effects influenced by natural selection may be an important factor which is causing diversification of expression patterns (rebalancing of expression) of duplicate genes in the course of fixation of gene duplications. This process is similar to the conventional dosage effect hypothesis [3]. After the gene duplication is fixed in a population, preservation of this gene duplication may be largely explained by the DDC model (maintenance of duplicate genes due to differential loss or reduction of expression in various tissues).
Mentions: Similar observations have been reported previously for paralogous genes in yeast [45] and fly [46]. Oakley and coworkers used a phylogenetic approach to demonstrate that the fast evolutionary rate of tissue-specific repression or loss of gene expression is significantly higher than the rate of activation or gain [46]. It was also found that DDC is consistent with only a portion of possible ancestral histories of gene expression [46]. 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. It was suggested that although the majority of the expression reduction is likely to be neutral, for some of duplicate genes, it could be beneficial through the rebalanced gene dosage [41].

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.

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.

No MeSH data available.


Related in: MedlinePlus