Dataset Information

Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates.

ABSTRACT: Mammalian and avian genomes are characterized by a substantial spatial heterogeneity of GC-content, which is often interpreted as reflecting the effect of local GC-biased gene conversion (gBGC), a meiotic repair bias that favors G and C over A and T alleles in high-recombining genomic regions. Surprisingly, the first fully sequenced nonavian sauropsid (i.e., reptile), the green anole Anolis carolinensis, revealed a highly homogeneous genomic GC-content landscape, suggesting the possibility that gBGC might not be at work in this lineage. Here, we analyze GC-content evolution at third-codon positions (GC3) in 44 vertebrates species, including eight newly sequenced transcriptomes, with a specific focus on nonavian sauropsids. We report that reptiles, including the green anole, have a genome-wide distribution of GC3 similar to that of mammals and birds, and we infer a strong GC3-heterogeneity to be already present in the tetrapod ancestor. We further show that the dynamic of coding sequence GC-content is largely governed by karyotypic features in vertebrates, notably in the green anole, in agreement with the gBGC hypothesis. The discrepancy between third-codon positions and noncoding DNA regarding GC-content dynamics in the green anole could not be explained by the activity of transposable elements or selection on codon usage. This analysis highlights the unique value of third-codon positions as an insertion/deletion-free marker of nucleotide substitution biases that ultimately affect the evolution of proteins.

SUBMITTER: Figuet E

PROVIDER: S-EPMC4316630 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates.

Figuet Emeric E Ballenghien Marion M Romiguier Jonathan J Galtier Nicolas N

Genome biology and evolution 20141219 1

Mammalian and avian genomes are characterized by a substantial spatial heterogeneity of GC-content, which is often interpreted as reflecting the effect of local GC-biased gene conversion (gBGC), a meiotic repair bias that favors G and C over A and T alleles in high-recombining genomic regions. Surprisingly, the first fully sequenced nonavian sauropsid (i.e., reptile), the green anole Anolis carolinensis, revealed a highly homogeneous genomic GC-content landscape, suggesting the possibility that ...[more]

PMID: 25527834

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Project description:The characterization of functional elements in genomes relies on the identification of the footprints of natural selection. In this quest, taking into account neutral evolutionary processes such as mutation and genetic drift is crucial because these forces can generate patterns that may obscure or mimic signatures of selection. In mammals, and probably in many eukaryotes, another such confounding factor called GC-Biased Gene Conversion (gBGC) has been documented. This mechanism generates patterns identical to what is expected under selection for higher GC-content, specifically in highly recombining genomic regions. Recent results have suggested that a mysterious selective force favouring higher GC-content exists in Bacteria but the possibility that it could be gBGC has been excluded. Here, we show that gBGC is probably at work in most if not all bacterial species. First we find a consistent positive relationship between the GC-content of a gene and evidence of intra-genic recombination throughout a broad spectrum of bacterial clades. Second, we show that the evolutionary force responsible for this pattern is acting independently from selection on codon usage, and could potentially interfere with selection in favor of optimal AU-ending codons. A comparison with data from human populations shows that the intensity of gBGC in Bacteria is comparable to what has been reported in mammals. We propose that gBGC is not restricted to sexual Eukaryotes but also widespread among Bacteria and could therefore be an ancestral feature of cellular organisms. We argue that if gBGC occurs in bacteria, it can account for previously unexplained observations, such as the apparent non-equilibrium of base substitution patterns and the heterogeneity of gene composition within bacterial genomes. Because gBGC produces patterns similar to positive selection, it is essential to take this process into account when studying the evolutionary forces at work in bacterial genomes.

Project description:We examined seventy million well-characterized human mutations, and their impact on G+C-compositional dynamics, in order to understand the formation and maintenance of major genomic nucleotide sequence patterns. Among novel mutations, those that change a strong (S) base pair G:C/C:G to a weak (W) pair A:T/T:A occur at nearly twice the frequency of the opposite mutations. Such imbalance puts strong downward pressure on overall GC-content. However, along protracted paths to fixation, S?W mutations are much less likely to propagate than W?S mutations. The magnitude of relative propagation disadvantages for S?W mutations is inexplicable by any currently-accepted model. This fact forced us to re-examine the quantitative features of Biased Gene Conversion (BGC) theory. Revised parameters of BGC that, per average individual, convert 7-14 W base pairs into S pairs, would account for the S-content turnover differences between new and old mutations, and make BGC an instrumental force for nucleotide dynamics and evolution. BGC should thus be considered seriously in both theories and biomedical practice. In particular, BGC should be taken into account during allele imputations, where missing SNP alleles are computationally predicted based on the information about several neighboring alleles. Finally, we analyzed the effect of neighboring nucleotide context on the mutation frequencies, dynamics, and GC-composition turnover. For this purpose, we examined genomic regions having extremely biased nucleotide compositions (enriched for S-, W-, purine/pyrimidine strand asymmetry, or AC/GT-strand asymmetry). It was found that point mutations in these regions preferentially degrade the nucleotide inhomogeneities, decreasing the sequence biases. Degradation of sequence bias is highest for novel mutations, and considerably lower for older mutations (those widespread across populations). Besides BGC, there may be additional, still uncharacterized molecular mechanisms that either preserve genomic regions with biased nucleotide compositions from mutational degradation or fail to degrade such inhomogeneities in specific chromosomal regions.

Dataset Information

Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates.

Publications

Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates.

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