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Gene family size conservation is a good indicator of evolutionary rates.

Chen FC, Chen CJ, Li WH, Chuang TJ - Mol. Biol. Evol. (2010)

Bottom Line: In addition, we show that the duplicate genes with family size conservation evolve significantly more slowly than those without family size conservation.Our results thus suggest that the controversy on whether duplicate genes evolve more slowly than singletons can be resolved when family size conservation is taken into consideration.Our results thus point to the importance of family size conservation in the evolution of duplicate genes.

View Article: PubMed Central - PubMed

Affiliation: Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences, National Health Research Institutes, Miaoli County, Taiwan.

ABSTRACT
The evolution of duplicate genes has been a topic of broad interest. Here, we propose that the conservation of gene family size is a good indicator of the rate of sequence evolution and some other biological properties. By comparing the human-chimpanzee-macaque orthologous gene families with and without family size conservation, we demonstrate that genes with family size conservation evolve more slowly than those without family size conservation. Our results further demonstrate that both family expansion and contraction events may accelerate gene evolution, resulting in elevated evolutionary rates in the genes without family size conservation. In addition, we show that the duplicate genes with family size conservation evolve significantly more slowly than those without family size conservation. Interestingly, the median evolutionary rate of singletons falls in between those of the above two types of duplicate gene families. Our results thus suggest that the controversy on whether duplicate genes evolve more slowly than singletons can be resolved when family size conservation is taken into consideration. Furthermore, we also observe that duplicate genes with family size conservation have the highest level of gene expression/expression breadth, the highest proportion of essential genes, and the lowest gene compactness, followed by singletons and then by duplicate genes without family size conservation. Such a trend accords well with our observations of evolutionary rates. Our results thus point to the importance of family size conservation in the evolution of duplicate genes.

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The left panel compares (A) the proportions of essential genes, (C) the expression levels, (E) the expression breadth, and (G) the gene compactness (average intron/UTR length) between gene families with and without size conservation (“H=C=M” and “non-H=C=M,” respectively). The right panel (B, D, F, and H) compares the four same features in the same order between singleton gene families with size conservation (“H=C=M=1”) and multigene families with or without size conservation (“H=C=M>1” and “dup-H≠C≠M,” respectively). The P values were estimated by using the two-tailed Fisher’s exact test (A, B, E, and F), the two-tailed Wilcoxon rank sum test (C and D), and the two-tailed t-test (G and H). NS, not significant.
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fig3: The left panel compares (A) the proportions of essential genes, (C) the expression levels, (E) the expression breadth, and (G) the gene compactness (average intron/UTR length) between gene families with and without size conservation (“H=C=M” and “non-H=C=M,” respectively). The right panel (B, D, F, and H) compares the four same features in the same order between singleton gene families with size conservation (“H=C=M=1”) and multigene families with or without size conservation (“H=C=M>1” and “dup-H≠C≠M,” respectively). The P values were estimated by using the two-tailed Fisher’s exact test (A, B, E, and F), the two-tailed Wilcoxon rank sum test (C and D), and the two-tailed t-test (G and H). NS, not significant.

Mentions: Because essential genes are known to evolve slowly (Wall et al. 2005; Zhang and He 2005; Liao et al. 2006; Larracuente et al. 2008), we then ask whether the member genes of size-conserved families tend to be essential. Accordingly, we compare the proportion of essential genes (including human essential genes [Liao and Zhang 2008] and human orthologues of mouse lethal genes [Liao and Zhang 2007]) between the H=C=M families and the non-H=C=M families. Figure 3A shows that the genes of H=C=M families have a significantly higher proportion of essential genes than those of non-H=C=M families for both data sets (both P values < 0.05). Subsequently, we probe the relationship between gene essentiality and gene duplicability. Figure 3B shows that the genes of H=C=M>1 families have a significantly higher proportion of essential genes (for both essential gene data sets) than those of singletons (both P values < 0.05). If the factor of family size conservation is not considered, the difference in the proportion of essential genes between singletons and duplicate genes becomes statistically insignificant (P values > 0.5 for both data sets by the two-tailed Fisher’s exact test). Interestingly, this observation is consistent with the previous reports that gene essentiality and gene duplicability are uncorrelated in mammals (Liang and Li 2007; Liao and Zhang 2007). Our result thus suggests that the apparent lack of correlation between gene essentiality and duplicability may not be true, supporting a recent claim that gene duplicability and essentiality are correlated after controlling for confounding factors (Liang and Li 2009). Furthermore, our analysis shows that families with size conservation tend to be more functionally important than those without size conservation. In fact, the H=C=M>1 families have the highest percentage of essential genes, followed by the H=C=M=1 families, and then by dup-H≠C≠M families (fig. 3B). The overall trend accords well with what we observe in the analysis of evolutionary rates (table 4).


Gene family size conservation is a good indicator of evolutionary rates.

Chen FC, Chen CJ, Li WH, Chuang TJ - Mol. Biol. Evol. (2010)

The left panel compares (A) the proportions of essential genes, (C) the expression levels, (E) the expression breadth, and (G) the gene compactness (average intron/UTR length) between gene families with and without size conservation (“H=C=M” and “non-H=C=M,” respectively). The right panel (B, D, F, and H) compares the four same features in the same order between singleton gene families with size conservation (“H=C=M=1”) and multigene families with or without size conservation (“H=C=M>1” and “dup-H≠C≠M,” respectively). The P values were estimated by using the two-tailed Fisher’s exact test (A, B, E, and F), the two-tailed Wilcoxon rank sum test (C and D), and the two-tailed t-test (G and H). NS, not significant.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2908708&req=5

fig3: The left panel compares (A) the proportions of essential genes, (C) the expression levels, (E) the expression breadth, and (G) the gene compactness (average intron/UTR length) between gene families with and without size conservation (“H=C=M” and “non-H=C=M,” respectively). The right panel (B, D, F, and H) compares the four same features in the same order between singleton gene families with size conservation (“H=C=M=1”) and multigene families with or without size conservation (“H=C=M>1” and “dup-H≠C≠M,” respectively). The P values were estimated by using the two-tailed Fisher’s exact test (A, B, E, and F), the two-tailed Wilcoxon rank sum test (C and D), and the two-tailed t-test (G and H). NS, not significant.
Mentions: Because essential genes are known to evolve slowly (Wall et al. 2005; Zhang and He 2005; Liao et al. 2006; Larracuente et al. 2008), we then ask whether the member genes of size-conserved families tend to be essential. Accordingly, we compare the proportion of essential genes (including human essential genes [Liao and Zhang 2008] and human orthologues of mouse lethal genes [Liao and Zhang 2007]) between the H=C=M families and the non-H=C=M families. Figure 3A shows that the genes of H=C=M families have a significantly higher proportion of essential genes than those of non-H=C=M families for both data sets (both P values < 0.05). Subsequently, we probe the relationship between gene essentiality and gene duplicability. Figure 3B shows that the genes of H=C=M>1 families have a significantly higher proportion of essential genes (for both essential gene data sets) than those of singletons (both P values < 0.05). If the factor of family size conservation is not considered, the difference in the proportion of essential genes between singletons and duplicate genes becomes statistically insignificant (P values > 0.5 for both data sets by the two-tailed Fisher’s exact test). Interestingly, this observation is consistent with the previous reports that gene essentiality and gene duplicability are uncorrelated in mammals (Liang and Li 2007; Liao and Zhang 2007). Our result thus suggests that the apparent lack of correlation between gene essentiality and duplicability may not be true, supporting a recent claim that gene duplicability and essentiality are correlated after controlling for confounding factors (Liang and Li 2009). Furthermore, our analysis shows that families with size conservation tend to be more functionally important than those without size conservation. In fact, the H=C=M>1 families have the highest percentage of essential genes, followed by the H=C=M=1 families, and then by dup-H≠C≠M families (fig. 3B). The overall trend accords well with what we observe in the analysis of evolutionary rates (table 4).

Bottom Line: In addition, we show that the duplicate genes with family size conservation evolve significantly more slowly than those without family size conservation.Our results thus suggest that the controversy on whether duplicate genes evolve more slowly than singletons can be resolved when family size conservation is taken into consideration.Our results thus point to the importance of family size conservation in the evolution of duplicate genes.

View Article: PubMed Central - PubMed

Affiliation: Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences, National Health Research Institutes, Miaoli County, Taiwan.

ABSTRACT
The evolution of duplicate genes has been a topic of broad interest. Here, we propose that the conservation of gene family size is a good indicator of the rate of sequence evolution and some other biological properties. By comparing the human-chimpanzee-macaque orthologous gene families with and without family size conservation, we demonstrate that genes with family size conservation evolve more slowly than those without family size conservation. Our results further demonstrate that both family expansion and contraction events may accelerate gene evolution, resulting in elevated evolutionary rates in the genes without family size conservation. In addition, we show that the duplicate genes with family size conservation evolve significantly more slowly than those without family size conservation. Interestingly, the median evolutionary rate of singletons falls in between those of the above two types of duplicate gene families. Our results thus suggest that the controversy on whether duplicate genes evolve more slowly than singletons can be resolved when family size conservation is taken into consideration. Furthermore, we also observe that duplicate genes with family size conservation have the highest level of gene expression/expression breadth, the highest proportion of essential genes, and the lowest gene compactness, followed by singletons and then by duplicate genes without family size conservation. Such a trend accords well with our observations of evolutionary rates. Our results thus point to the importance of family size conservation in the evolution of duplicate genes.

Show MeSH
Related in: MedlinePlus