Abstract
A strong correlation between GC content and recombination rate is observed in many eukaryotes, which is thought to be due to conversion events linked to the repair of meiotic double-strand breaks. In several organisms, the length of conversion tracts has been shown to decrease exponentially with increasing distance from the sites of meiotic double-strand breaks. I show here that this behavior leads to a simple analytical model for the evolution and the equilibrium state of the GC content of sequences devoid of meiotic double-strand break sites. In the yeast Saccharomyces cerevisiae, meiotic double-strand breaks are practically excluded from protein-coding sequences. A good fit was observed between the predictions of the model and the variations of the average GC content of the third codon position (GC3) of S. cerevisiae genes. Moreover, recombination parameters that can be extracted by fitting the data to the model coincide with experimentally determined values. These results thus indicate that meiotic recombination plays an important part in determining the fluctuations of GC content in yeast coding sequences. The model also accounted for the different patterns of GC variations observed in the genes of Candida species that exhibit a variety of sexual lifestyles, and hence a wide range of meiotic recombination rates. Finally, the variations of the average GC3 content of human and chicken coding sequences could also be fitted by the model. These results suggest the existence of a widespread pattern of GC variation in eukaryotic genes due to meiotic recombination, which would imply the generality of two features of meiotic recombination: its association with GC-biased gene conversion and the quasi-exclusion of meiotic double-strand breaks from coding sequences. Moreover, the model points out to specific constraints on protein fragments encoded by exon terminal sequences, which are the most affected by the GC bias.
Highlights
Almost ubiquitous among eukaryotic organisms is a correlation between GC content and meiotic recombination rates [1,2,3,4,5]
This mechanism relies on the fact that during meiotic recombination, double-strand breaks (DSBs) are repaired through a process involving the formation of DNA heteroduplexes between the strands of the cut and the uncut chromosomes
We will suppose that this process involves two kinds of mechanisms: (i) mechanisms dependent on meiotic recombination, which modify the probability of fixation of an allele through gene conversion and (ii) mechanisms independent of meiotic recombination, which operate uniformly on the segments of the sequence, independently of their positions x
Summary
Almost ubiquitous among eukaryotic organisms is a correlation between GC content and meiotic recombination rates [1,2,3,4,5]. Whereas the causality relationships are debated in many cases, several lines of evidence have accumulated for a mechanism termed GC-biased gene conversion whereby the frequency of meiotic recombination affects the evolution of GC content (for a review, see [6]). This mechanism relies on the fact that during meiotic recombination, double-strand breaks (DSBs) are repaired through a process involving the formation of DNA heteroduplexes between the strands of the cut and the uncut chromosomes (see [7,8] for reviews). The fact that crossovers are frequently associated with simple, continuous conversion tracts indicates that in the majority of the cases the sequence of the cut chromosome is systematically converted [9]
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