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. 2004 Mar;2(3):E55.
doi: 10.1371/journal.pbio.0020055. Epub 2004 Mar 16.

Preferential duplication of conserved proteins in eukaryotic genomes

Jerel C Davis  1 , Dmitri A Petrov
Affiliations

Preferential duplication of conserved proteins in eukaryotic genomes

Jerel C Davis et al. PLoS Biol. 2004 Mar.

Abstract

A central goal in genome biology is to understand the origin and maintenance of genic diversity. Over evolutionary time, each gene's contribution to the genic content of an organism depends not only on its probability of long-term survival, but also on its propensity to generate duplicates that are themselves capable of long-term survival. In this study we investigate which types of genes are likely to generate functional and persistent duplicates. We demonstrate that genes that have generated duplicates in the C. elegans and S. cerevisiae genomes were 25%-50% more constrained prior to duplication than the genes that failed to leave duplicates. We further show that conserved genes have been consistently prolific in generating duplicates for hundreds of millions of years in these two species. These findings reveal one way in which gene duplication shapes the content of eukaryotic genomes. Our finding that the set of duplicate genes is biased has important implications for genome-scale studies.

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Conflict of interest statement

The authors have declared that no conflicts of interest exist.

Figures

Figure 1
Figure 1. The Approach Used to Estimate the Rate of Evolution for Duplicate and Singleton Genes
For each duplicate (gray lines) and singleton (black lines) gene/pair in S. cerevisiae and C. elegans, unduplicated orthologs were identified in D. melanogaster and A. gambiae. The K A between this representative pair of orthologs was taken as an estimate of the rate of evolution of duplicate and singleton genes in the study species that is independent of the effects of duplication on molecular evolution.
Figure 2
Figure 2. A Comparison of the Evolutionary Rates of Duplicate and Singleton Genes
The average rate of nonsynonymous evolution (K A) for representative pairs of duplicate and singleton genes in the two study organisms S. cerevisiae (A) and C. elegans (B) is shown. Representative pairs of duplicate genes evolve significantly more slowly in both study organisms (Mann–Whitney U test, p < 0.001).
Figure 3
Figure 3. A Comparison of the Rate of Structural Evolution for Duplicate and Singleton Genes
For each representative pair, the number of gaps per aligned nucleotide was calculated. For both S. cerevisiae (A) and C. elegans (B), representative pairs of duplicates have significantly fewer insertions per basepair than representative pairs for singletons (Mann–Whitney U test, p < 0.0001 for both).
Figure 4
Figure 4. The Codon Bias and Rate of Evolution of Genes Leading to Duplicates over the Evolutionary History of S. cerevisiae and C. elegans
For both S. cerevisiae (A) and C. elegans (B), moving averages of nonsynonymous substitutions per site (K A, in dark gray), codon bias in the study organism (measured with CAI, in black), and codon bias of the representative ortholog in D. melanogaster (CAI, in light gray) are plotted against the number of synonymous substitutions per site (K S) between duplicate pairs. The bin size is 15, and standard error bars are shown. Dashed lines represent the average CAI of singleton genes and the average K A of representative pairs of singleton genes.
Figure 5
Figure 5. Correcting for Synonymous Substitutions Reveals That S. cerevisiae Genes That Have Recently Duplicated Have a Higher Codon Bias and Slower Rate of Evolution Than Those That Duplicated in the Ancient Past
For duplicate genes in S. cerevisiae, moving averages of the number of nonsynonymous substitutions per nonsynonymous site of representative pairs (K A, in dark gray), the codon bias in S. cerevisiae (CAI, in black), and the codon bias of representative pairs in D. melanogaster (CAI, in light gray) are plotted against the adjusted number of synonymous substitutions per site (see Materials and Methods) between duplicate pairs. The bin size is 15, and standard error bars are shown. Lines with broad dashes show the respective averages for singleton genes in S. cerevisiae, and the line with short dashes shows the average K A for representative pairs of duplicate genes in C. elegans.
Figure 6
Figure 6. After Removing Ribosomal Genes, the Magnitude of the Bias towards the Slower Evolution of Duplicate Genes Is Similar in Both S. cerevisiae and C. elegans
For nonribosomal duplicate genes in S. cerevisiae, moving averages of the number of nonsynonymous substitutions per nonsynonymous site of representative pairs (K A, in dark gray), the codon bias in S. cerevisiae (CAI, in black), and the codon bias of representative pairs in D. melanogaster (CAI, in light gray) are plotted against the adjusted number of synonymous substitutions per site (see Materials and Methods) between duplicate pairs. The bin size is 15, and standard error bars are shown. Lines with broad dashes show the respective averages for singleton genes in S. cerevisiae, and the line with short dashes shows the average K A for representative pairs of duplicate genes in C. elegans.
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