X-Linked Genes Evolve Higher Codon Bias in Drosophila and Caenorhabditis

Singh, Nadia D.; Davis, Jerel C.; Petrov, Dmitri A.

doi:10.1534/genetics.105.043497

Cited by 62 publications

(71 citation statements)

References 54 publications

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“…It has recently been reported that X-chromosomal genes have a higher codon bias than autosomal genes (Singh et al 2005). We observed that DCC target genes have a higher expression than nontargets.…”

Section: Dna Sequence Elements May Attract the DCC To Target Genessupporting

confidence: 47%

Chromosome-wide gene-specific targeting of theDrosophiladosage compensation complex

Gilfillan¹,

Straub²,

Wit³

et al. 2006

Genes Dev.

147

209

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The dosage compensation complex (DCC) of Drosophila melanogaster is capable of distinguishing the single male X from the other chromosomes in the nucleus. It selectively interacts in a discontinuous pattern with much of the X chromosome. How the DCC identifies and binds the X, including binding to the many genes that require dosage compensation, is currently unknown. To identify bound genes and attempt to isolate the targeting cues, we visualized male-specific lethal 1 (MSL1) protein binding along the X chromosome by combining chromatin immunoprecipitation with high-resolution microarrays. More than 700 binding regions for the DCC were observed, encompassing more than half the genes found on the X chromosome. In addition, several rare autosomal binding sites were identified. Essential genes are preferred targets, and genes binding high levels of DCC appear to experience the most compensation (i.e., greatest increase in expression). DCC binding clearly favors genes over intergenic regions, and binds most strongly to the 3 end of transcription units. Within the targeted genes, the DCC exhibits a strong preference for exons and coding sequences. Our results demonstrate gene-specific binding of the DCC, and identify several sequence elements that may partly direct its targeting.[Keywords: Transcription; histone modification; chromatin remodeling; MSL complex; microarray; gene expression] Supplemental material is available at http://www.genesdev.org.

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Section: Dna Sequence Elements May Attract the DCC To Target Genessupporting

confidence: 47%

Chromosome-wide gene-specific targeting of theDrosophiladosage compensation complex

Gilfillan¹,

Straub²,

Wit³

et al. 2006

Genes Dev.

147

209

View full text Add to dashboard Cite

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“…At least one gene in our study, ry, shows strong gene-specific patterns of codon bias evolution in several lineages. Singh et al (2005) have shown elevated codon bias on Drosophila X chromosomes relative to autosomes and increases in GC content were noted by Takano-Shimizu (1999 for genes on the tip (telomeric region) of the X chromosome in the D. teissieri-D. yakuba and D. erecta-D. orena clades. These departures appear to be region specific; genes in the present analysis show a decline of preferred codon usage in lineages showing strong GC increases at the tip of the X chromosome.…”

Section: Discussionmentioning

confidence: 75%

Molecular Evolution in the Drosophila melanogaster Species Subgroup: Frequent Parameter Fluctuations on the Timescale of Molecular Divergence

Akashi

Piao

et al. 2006

Genetics

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Although mutation, genetic drift, and natural selection are well established as determinants of genome evolution, the importance (frequency and magnitude) of parameter fluctuations in molecular evolution is less understood. DNA sequence comparisons among closely related species allow specific substitutions to be assigned to lineages on a phylogenetic tree. In this study, we compare patterns of codon usage and protein evolution in 22 genes (.11,000 codons) among Drosophila melanogaster and five relatives within the D. melanogaster subgroup. We assign changes to eight lineages using a maximum-likelihood approach to infer ancestral states. Uncertainty in ancestral reconstructions is taken into account, at least to some extent, by weighting reconstructions by their posterior probabilities. Four of the eight lineages show potentially genomewide departures from equilibrium synonymous codon usage; three are decreasing and one is increasing in major codon usage. Several of these departures are consistent with lineage-specific changes in selection intensity (selection coefficients scaled to effective population size) at silent sites. Intron base composition and rates and patterns of protein evolution are also heterogeneous among these lineages. The magnitude of forces governing silent, intron, and protein evolution appears to have varied frequently, and in a lineage-specific manner, within the D. melanogaster subgroup. U NDERSTANDING the forces governing the origins and evolutionary fates of DNA mutations is central to the study of molecular evolution. A great deal of attention has been focused on determining the relative contributions of genetic drift and natural selection to patterns of divergence among genomes (reviewed in Ohta 2002). However, the magnitude, timescale, and genomic breadth of fluctuations in molecular evolutionary forces remain to be studied systematically. Such knowledge is critical for modeling the causes of molecular evolution and is necessary for designing tests of adaptive and deleterious evolution and methods for phylogenetic inference and ancestral state reconstruction.Determinants of molecular evolution include mutation rates and patterns, effective population sizes, rates of recombination and biased gene conversion, and the fitness effects of mutations. Strict constancy of all these factors is implausible. However, the timescale of parameter fluctuations determines their relevance to molecular evolution; variability in evolutionary forces cause heterogeneous substitution patterns if parameters changes occur on a similar timescale as molecular evolution (Gillespie 1993(Gillespie , 1994 Cutler 2000a,b). Although theoretical concerns suggest that appropriately scaled parameter fluctuations should not be common, numerous studies have invoked nonstationarity to explain variable rates of protein evolution at particular loci or in specific lineages. These include fluctuations in neutral mutation rates (Fitch and Markowitz 1970;Fitch 1971;Takahata 1987), effective population sizes (e.g., Oht...

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“…1 (Table 3 and Singh et al, 2005). This is much larger than the maximum value predicted by McVean & Charlesworth (1999), who assumed that the effective population size N e for the X (N eX ) is three-quarters of that for the autosomes (N eA ).…”

Section: Discussionmentioning

confidence: 79%

“…As we discuss in the next section, another (not mutually exclusive) possibility is that differences in effective population size between the X chromosome and the autosomes could be increasing the level of codon usage bias on the X. Singh et al (2005) estimated codon bias levels in D. melanogaster, D. pseudoobscura and Caenorhabditis elegans and found that these were higher on the X chromosome than on the autosomes in all three species. They excluded other factors that are correlated with codon usage bias, such as gene expression, gene length, recombination rate, gene density and protein evolution as possible causes for the X-autosome difference, suggesting that more efficient selection on the hemizygous male X is the main cause of increased codon usage bias on the X.…”

Section: Discussionmentioning

confidence: 99%

A multispecies approach for comparing sequence evolution of X-linked and autosomal sites inDrosophila

Vicoso

Haddrill²,

Charlesworth

2008

Genet. Res.

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This version is available at https://strathprints.strath.ac.uk/47568/ Strathprints is designed to allow users to access the research output of the University of Strathclyde. Unless otherwise explicitly stated on the manuscript, Copyright © and Moral Rights for the papers on this site are retained by the individual authors and/or other copyright owners. Please check the manuscript for details of any other licences that may have been applied. You may not engage in further distribution of the material for any profitmaking activities or any commercial gain. You may freely distribute both the url (https://strathprints.strath.ac.uk/) and the content of this paper for research or private study, educational, or not-for-profit purposes without prior permission or charge.Any correspondence concerning this service should be sent to the SummaryPopulation genetics models show that, under certain conditions, the X chromosome is expected to be under more efficient selection than the autosomes. This could lead to 'faster-X evolution ', if a large proportion of mutations are fixed by positive selection, as suggested by recent studies in Drosophila. We used a multispecies approach to test this : Muller's element D, an autosomal arm, is fused to the ancestral X chromosome in Drosophila pseudoobscura and its sister species, Drosophila affinis. We tested whether the same set of genes had higher rates of non-synonymous evolution when they were X-linked (in the D. pseudoobscura/D. affinis comparison) than when they were autosomal (in Drosophila melanogaster/Drosophila yakuba). Although not significant, our results suggest this may be the case, but only for genes under particularly strong positive selection/weak purifying selection. They also suggest that genes that have become X-linked have higher levels of codon bias and slower synonymous site evolution, consistent with more effective selection on codon usage at X-linked sites.

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X-Linked Genes Evolve Higher Codon Bias in Drosophila and Caenorhabditis

Cited by 62 publications

References 54 publications

Chromosome-wide gene-specific targeting of theDrosophiladosage compensation complex

Chromosome-wide gene-specific targeting of theDrosophiladosage compensation complex

Molecular Evolution in the Drosophila melanogaster Species Subgroup: Frequent Parameter Fluctuations on the Timescale of Molecular Divergence

A multispecies approach for comparing sequence evolution of X-linked and autosomal sites inDrosophila

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