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Tempo and mode of gene duplication in mammalian ribosomal protein evolution.

Dharia AP, Obla A, Gajdosik MD, Simon A, Nelson CE - PLoS ONE (2014)

Bottom Line: This result was surprising due to the fact that ribosomal protein genes evolve slowly and transcript levels are very tightly regulated.Furthermore, we conclude that existing gene duplication models do not readily account for the preservation of a very large number of intact retroduplicated ribosomal protein (RT-RP) genes observed in mammalian genomes.We suggest that selection against dominant-negative mutations may underlie the unexpected retention and conservation of duplicated RP genes, and may shape the fate of newly duplicated genes, regardless of duplication mechanism.

View Article: PubMed Central - PubMed

Affiliation: University of Connecticut Department of Molecular and Cell Biology, Storrs, Connecticut, United States of America.

ABSTRACT
Gene duplication has been widely recognized as a major driver of evolutionary change and organismal complexity through the generation of multi-gene families. Therefore, understanding the forces that govern the evolution of gene families through the retention or loss of duplicated genes is fundamentally important in our efforts to study genome evolution. Previous work from our lab has shown that ribosomal protein (RP) genes constitute one of the largest classes of conserved duplicated genes in mammals. This result was surprising due to the fact that ribosomal protein genes evolve slowly and transcript levels are very tightly regulated. In our present study, we identified and characterized all RP duplicates in eight mammalian genomes in order to investigate the tempo and mode of ribosomal protein family evolution. We show that a sizable number of duplicates are transcriptionally active and are very highly conserved. Furthermore, we conclude that existing gene duplication models do not readily account for the preservation of a very large number of intact retroduplicated ribosomal protein (RT-RP) genes observed in mammalian genomes. We suggest that selection against dominant-negative mutations may underlie the unexpected retention and conservation of duplicated RP genes, and may shape the fate of newly duplicated genes, regardless of duplication mechanism.

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RP gene duplicates in 8 mammalian genomes.A) Distribution of duplication events in 8 mammalian genomes. B) Assessment of coverage or species-specific bias in ribosomal protein gene duplicates. C) Representation of DNA and RNA-mediated duplications in RP gene families. Abbreviations: Hs, Homo sapiens (human); Pt, Pan troglodytes (chimpanzee); Mmul, Macaca mulatta (Rhesus macaque); Mm, Mus musculus (house mouse); Rn, Rattus norvegicus (Norway rat); Bt, Bos taurus (cattle); Cf, Canis familiaris (dog); Md, Monodelphis domestica (gray short-tailed opossum); Gg, gallus gallus (chicken).
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pone-0111721-g002: RP gene duplicates in 8 mammalian genomes.A) Distribution of duplication events in 8 mammalian genomes. B) Assessment of coverage or species-specific bias in ribosomal protein gene duplicates. C) Representation of DNA and RNA-mediated duplications in RP gene families. Abbreviations: Hs, Homo sapiens (human); Pt, Pan troglodytes (chimpanzee); Mmul, Macaca mulatta (Rhesus macaque); Mm, Mus musculus (house mouse); Rn, Rattus norvegicus (Norway rat); Bt, Bos taurus (cattle); Cf, Canis familiaris (dog); Md, Monodelphis domestica (gray short-tailed opossum); Gg, gallus gallus (chicken).

Mentions: The first step of our pipeline identified all detectable duplicates of RP genes in eight mammalian genomes. RP families included 14,552 gene duplicates in the eight genomes analyzed: human, chimp, monkey, mouse, rat, dog, cow, and opossum (Figure 2A). Although data in figure 2A include duplicates with shared ancestry, the counts for each species represent the number of duplicate genes present in each extant species. To determine if sequencing coverage had a significant impact on our detection of RP gene duplicates, we compared the depth of sequence coverage in each species' genome to the number of duplications recovered in that species. We found no significant correlation between the number of duplications and genome coverage (Pearson's r = −0.353, p = 0.391, Figure 2B, S2). We also tested for bias in duplication types in each species and found no species-specific bias in duplication mechanisms. As we found significant association between species (p = 6.07e-17, two-way chi square test, Figure2B), all species were grouped for subsequent analyses.


Tempo and mode of gene duplication in mammalian ribosomal protein evolution.

Dharia AP, Obla A, Gajdosik MD, Simon A, Nelson CE - PLoS ONE (2014)

RP gene duplicates in 8 mammalian genomes.A) Distribution of duplication events in 8 mammalian genomes. B) Assessment of coverage or species-specific bias in ribosomal protein gene duplicates. C) Representation of DNA and RNA-mediated duplications in RP gene families. Abbreviations: Hs, Homo sapiens (human); Pt, Pan troglodytes (chimpanzee); Mmul, Macaca mulatta (Rhesus macaque); Mm, Mus musculus (house mouse); Rn, Rattus norvegicus (Norway rat); Bt, Bos taurus (cattle); Cf, Canis familiaris (dog); Md, Monodelphis domestica (gray short-tailed opossum); Gg, gallus gallus (chicken).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4219774&req=5

pone-0111721-g002: RP gene duplicates in 8 mammalian genomes.A) Distribution of duplication events in 8 mammalian genomes. B) Assessment of coverage or species-specific bias in ribosomal protein gene duplicates. C) Representation of DNA and RNA-mediated duplications in RP gene families. Abbreviations: Hs, Homo sapiens (human); Pt, Pan troglodytes (chimpanzee); Mmul, Macaca mulatta (Rhesus macaque); Mm, Mus musculus (house mouse); Rn, Rattus norvegicus (Norway rat); Bt, Bos taurus (cattle); Cf, Canis familiaris (dog); Md, Monodelphis domestica (gray short-tailed opossum); Gg, gallus gallus (chicken).
Mentions: The first step of our pipeline identified all detectable duplicates of RP genes in eight mammalian genomes. RP families included 14,552 gene duplicates in the eight genomes analyzed: human, chimp, monkey, mouse, rat, dog, cow, and opossum (Figure 2A). Although data in figure 2A include duplicates with shared ancestry, the counts for each species represent the number of duplicate genes present in each extant species. To determine if sequencing coverage had a significant impact on our detection of RP gene duplicates, we compared the depth of sequence coverage in each species' genome to the number of duplications recovered in that species. We found no significant correlation between the number of duplications and genome coverage (Pearson's r = −0.353, p = 0.391, Figure 2B, S2). We also tested for bias in duplication types in each species and found no species-specific bias in duplication mechanisms. As we found significant association between species (p = 6.07e-17, two-way chi square test, Figure2B), all species were grouped for subsequent analyses.

Bottom Line: This result was surprising due to the fact that ribosomal protein genes evolve slowly and transcript levels are very tightly regulated.Furthermore, we conclude that existing gene duplication models do not readily account for the preservation of a very large number of intact retroduplicated ribosomal protein (RT-RP) genes observed in mammalian genomes.We suggest that selection against dominant-negative mutations may underlie the unexpected retention and conservation of duplicated RP genes, and may shape the fate of newly duplicated genes, regardless of duplication mechanism.

View Article: PubMed Central - PubMed

Affiliation: University of Connecticut Department of Molecular and Cell Biology, Storrs, Connecticut, United States of America.

ABSTRACT
Gene duplication has been widely recognized as a major driver of evolutionary change and organismal complexity through the generation of multi-gene families. Therefore, understanding the forces that govern the evolution of gene families through the retention or loss of duplicated genes is fundamentally important in our efforts to study genome evolution. Previous work from our lab has shown that ribosomal protein (RP) genes constitute one of the largest classes of conserved duplicated genes in mammals. This result was surprising due to the fact that ribosomal protein genes evolve slowly and transcript levels are very tightly regulated. In our present study, we identified and characterized all RP duplicates in eight mammalian genomes in order to investigate the tempo and mode of ribosomal protein family evolution. We show that a sizable number of duplicates are transcriptionally active and are very highly conserved. Furthermore, we conclude that existing gene duplication models do not readily account for the preservation of a very large number of intact retroduplicated ribosomal protein (RT-RP) genes observed in mammalian genomes. We suggest that selection against dominant-negative mutations may underlie the unexpected retention and conservation of duplicated RP genes, and may shape the fate of newly duplicated genes, regardless of duplication mechanism.

Show MeSH