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A simple model for the influence of meiotic conversion tracts on GC content.

Marsolier-Kergoat MC - PLoS ONE (2011)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et de Technologies de Saclay, CEA/Saclay, Gif-sur-Yvette, France. mcmk@cea.fr

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.

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Variations of GC3 content in human and in chicken protein-coding sequences.The mean GC3 contents  of 66-codon segments are plotted as a function either of the segment position  relative to the ATG (red solid line) or of the segment position  relative to the stop codon (blue solid line). For each position  or ,  or  are averaged over all the first coding exons or over all the last coding exons, respectively, of human (A) or chicken (B) protein-coding sequences. The dashed lines represent the mean theoretical values  (red) or  (blue). The values of  (or ) were calculated as functions of  (or ) and , using Equations 5 (or 6) with the estimates of , , ,  and  given in Table 3.
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pone-0016109-g007: Variations of GC3 content in human and in chicken protein-coding sequences.The mean GC3 contents of 66-codon segments are plotted as a function either of the segment position relative to the ATG (red solid line) or of the segment position relative to the stop codon (blue solid line). For each position or , or are averaged over all the first coding exons or over all the last coding exons, respectively, of human (A) or chicken (B) protein-coding sequences. The dashed lines represent the mean theoretical values (red) or (blue). The values of (or ) were calculated as functions of (or ) and , using Equations 5 (or 6) with the estimates of , , , and given in Table 3.

Mentions: The GC3 content of human coding sequences was analyzed by considering all the single-exon genes and either the first coding exon of intron-containing genes for , or the last coding exon of intron-containing genes for . As shown in Figure 7A, the average GC3 content of the exon segments exhibited a decreasing trend with increasing distance either from the ATG or from the stop codon. The estimates of the parameters obtained by fitting with Equation 5 and with Equation 6 are given in Table 3. The Pearson's correlation coefficients either between and the theoretical GC3 content calculated from Equation 5 or between and the theoretical GC3 content calculated from Equation 6 are equal to 0.28 (, ) and to 0.30 (, ), respectively.


A simple model for the influence of meiotic conversion tracts on GC content.

Marsolier-Kergoat MC - PLoS ONE (2011)

Variations of GC3 content in human and in chicken protein-coding sequences.The mean GC3 contents  of 66-codon segments are plotted as a function either of the segment position  relative to the ATG (red solid line) or of the segment position  relative to the stop codon (blue solid line). For each position  or ,  or  are averaged over all the first coding exons or over all the last coding exons, respectively, of human (A) or chicken (B) protein-coding sequences. The dashed lines represent the mean theoretical values  (red) or  (blue). The values of  (or ) were calculated as functions of  (or ) and , using Equations 5 (or 6) with the estimates of , , ,  and  given in Table 3.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3020949&req=5

pone-0016109-g007: Variations of GC3 content in human and in chicken protein-coding sequences.The mean GC3 contents of 66-codon segments are plotted as a function either of the segment position relative to the ATG (red solid line) or of the segment position relative to the stop codon (blue solid line). For each position or , or are averaged over all the first coding exons or over all the last coding exons, respectively, of human (A) or chicken (B) protein-coding sequences. The dashed lines represent the mean theoretical values (red) or (blue). The values of (or ) were calculated as functions of (or ) and , using Equations 5 (or 6) with the estimates of , , , and given in Table 3.
Mentions: The GC3 content of human coding sequences was analyzed by considering all the single-exon genes and either the first coding exon of intron-containing genes for , or the last coding exon of intron-containing genes for . As shown in Figure 7A, the average GC3 content of the exon segments exhibited a decreasing trend with increasing distance either from the ATG or from the stop codon. The estimates of the parameters obtained by fitting with Equation 5 and with Equation 6 are given in Table 3. The Pearson's correlation coefficients either between and the theoretical GC3 content calculated from Equation 5 or between and the theoretical GC3 content calculated from Equation 6 are equal to 0.28 (, ) and to 0.30 (, ), respectively.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et de Technologies de Saclay, CEA/Saclay, Gif-sur-Yvette, France. mcmk@cea.fr

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.

Show MeSH
Related in: MedlinePlus