Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

Abstract

Abstract. The patterns and processes of molecular evolution may differ between the X chromosome and the autosomes in Drosophila melanogaster. This may in part be due to differences in the effective population size between the two chromosome sets and in part to the hemizygosity of the X chromosome in Drosophila males. These and other factors may lead to differences both in the gene complements of the X and the autosomes and in the properties of the genes residing on those chromosomes. Here we show that codon bias and recombination rate are correlated strongly and negatively on the X chromosome, and that this correlation cannot be explained by indirect relationships with other known determinants of codon bias. This is in dramatic contrast to the weak positive correlation found on the autosomes. We explored possible explanations for these patterns, which required a comprehensive analysis of the relationships among multiple genetic properties such as protein length and expression level. This analysis highlights conserved features of coding sequence evolution on the X and the autosomes and illuminates interesting differences between these two chromosome sets.

Fine-Scale Heterogeneity in Crossover Rate in thegarnet-scallopedRegion of theDrosophila melanogasterX Chromosome

“…In contrast, codon bias (as measured by FOP; see Materials and Methods) is significantly negatively correlated with recombination rate as has been previously reported for the X chromosome (Singh et al 2005(Singh et al , 2009) at the 5-and 10-kb scales (r , 20.12, P , 0.04, both scales; Table 1). Although these two parameters are also negatively correlated to a similar degree at the 20-, 50-, and 100-kb scales, these correlations are not statistically significant, perhaps owing to the limited number of windows with these increased window sizes.…”

“…GC content was not significantly correlated with crossover rate for any window size (Table 1). This is unexpected given that previous work reported a significant relationship between these two features on the X chromosome of D. melanogaster, a relationship that does not appear to be exclusively driven by GC content in regions of severely depressed rates of crossing over (Singh et al 2005). However, previous analysis of the fine-scale correlation between GC content and crossover rate (Singh et al 2009) also failed to recover the expected negative correlation between these two features.…”

Contrasting patterns of sequence divergence and base composition betweenDrosophilaintrons and intergenic regions

“…In INs, recombination rate neither correlates with the frequency of AT/GC and GC/ AT changes (rZK0.019, pZ0.681 and rZ0.054, pZ0.122, respectively) nor with GC content (rZK0.086, pZ0.362). The situation is distinctly different for IGs, where recombination rate shows a significantly positive correlation with the frequency of AT/GC polymorphisms (rZ0.099, pZ0.042; for Drosophila Singh et al 2005). The first observation suggests a recombination-associated fixation bias for GC polymorphisms (e.g.…”

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

“…Expression level and codon bias are strongly positively correlated (reviewed in Akashi 2001; see also Sharp and Li 1986;Bulmer 1988;Duret and Mouchiroud 1999;Hey and Kliman 2002), which likely reflects increased selective benefits of translational efficiency for highly expressed genes. In particular, EST counts in D. melanogaster and SAGE estimates in C. elegans correlate positively with FOP on both the X and the autosomes (Singh et al 2005).To examine the possibility that codon bias of X-linked genes is elevated because of increased expression level, we compared levels of gene expression between the X and the autosomes for the two systems for which gene expression data were available: D. melanogaster and C. elegans. Using EST counts as a metric of overall expression for genes in D. melanogaster, we found that X-linked genes are expressed at significantly lower levels than autosomal genes (EST counts are 7.5 and 11.7 for the X and the autosomes, respectively; P > 0.0001, two-tailed t-test).…”