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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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Ribosomal Protein Family duplication events based on age.All RP gene duplication events are displayed for 8 mammalian species. The bar charts at all speciation nodes show events classified by fate of duplication. The duplication counts on the bar charts are log normalized. RT-RPs are shown in red and RΨ-RPs in green. DD-RPs are not shown due to a very small sample size. The numbers above the bar charts represent the total number of gene duplication events at that speciation node. Age is marked at the bottom of the tree in millions of years (age estimates from [55], [103]).
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pone-0111721-g004: Ribosomal Protein Family duplication events based on age.All RP gene duplication events are displayed for 8 mammalian species. The bar charts at all speciation nodes show events classified by fate of duplication. The duplication counts on the bar charts are log normalized. RT-RPs are shown in red and RΨ-RPs in green. DD-RPs are not shown due to a very small sample size. The numbers above the bar charts represent the total number of gene duplication events at that speciation node. Age is marked at the bottom of the tree in millions of years (age estimates from [55], [103]).

Mentions: In the second step of our pipeline, we determined the probable location of each RP duplication event in evolutionary history of these eight species, and distinguished between RNA- and DNA-mediated duplication events (Figure 3; [18]). Based on our methodology, Figure 4 clearly shows that the majority of detectable duplications have occurred during recent mammalian evolution: 100 million years ago (MYA) or more recently. However, a significant number of duplications date between 100–300 MYA. The majority of RP gene duplications older than 90 MYA result in RNA-mediated pseudogenes (RΨ-RPs) (190), though some events (25) are intact RNA-mediated duplications (RT-RPs), and a very small number (4) are linked to intact DNA-mediated duplicates (DD-RPs) [data not shown for DD-RPS due to small sample size]. It is important to note that many of the more ancient duplications detected represent incomplete clades; therefore we infer a considerable amount of gene loss. However, our inability to detect these genes may also be due to loss of synteny or other limitations of our pipeline.


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

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

Ribosomal Protein Family duplication events based on age.All RP gene duplication events are displayed for 8 mammalian species. The bar charts at all speciation nodes show events classified by fate of duplication. The duplication counts on the bar charts are log normalized. RT-RPs are shown in red and RΨ-RPs in green. DD-RPs are not shown due to a very small sample size. The numbers above the bar charts represent the total number of gene duplication events at that speciation node. Age is marked at the bottom of the tree in millions of years (age estimates from [55], [103]).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0111721-g004: Ribosomal Protein Family duplication events based on age.All RP gene duplication events are displayed for 8 mammalian species. The bar charts at all speciation nodes show events classified by fate of duplication. The duplication counts on the bar charts are log normalized. RT-RPs are shown in red and RΨ-RPs in green. DD-RPs are not shown due to a very small sample size. The numbers above the bar charts represent the total number of gene duplication events at that speciation node. Age is marked at the bottom of the tree in millions of years (age estimates from [55], [103]).
Mentions: In the second step of our pipeline, we determined the probable location of each RP duplication event in evolutionary history of these eight species, and distinguished between RNA- and DNA-mediated duplication events (Figure 3; [18]). Based on our methodology, Figure 4 clearly shows that the majority of detectable duplications have occurred during recent mammalian evolution: 100 million years ago (MYA) or more recently. However, a significant number of duplications date between 100–300 MYA. The majority of RP gene duplications older than 90 MYA result in RNA-mediated pseudogenes (RΨ-RPs) (190), though some events (25) are intact RNA-mediated duplications (RT-RPs), and a very small number (4) are linked to intact DNA-mediated duplicates (DD-RPs) [data not shown for DD-RPS due to small sample size]. It is important to note that many of the more ancient duplications detected represent incomplete clades; therefore we infer a considerable amount of gene loss. However, our inability to detect these genes may also be due to loss of synteny or other limitations of our pipeline.

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