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Population genomics of the fission yeast Schizosaccharomyces pombe.

Fawcett JA, Iida T, Takuno S, Sugino RP, Kado T, Kugou K, Mura S, Kobayashi T, Ohta K, Nakayama J, Innan H - PLoS ONE (2014)

Bottom Line: In addition to introns and untranslated regions (UTRs), intergenic regions also exhibited lower levels of nucleotide diversity than synonymous sites, suggesting that a considerable amount of noncoding DNA is under selective constraint and thus likely to be functional.A number of genomic regions showed a reduction of nucleotide diversity probably caused by selective sweeps.Our study should serve as an important starting point in using a population genomics approach to further elucidate the biology of this important model organism.

View Article: PubMed Central - PubMed

Affiliation: Graduate University for Advanced Studies, Hayama, Kanagawa, Japan.

ABSTRACT
The fission yeast Schizosaccharomyces pombe has been widely used as a model eukaryote to study a diverse range of biological processes. However, population genetic studies of this species have been limited to date, and we know very little about the evolutionary processes and selective pressures that are shaping its genome. Here, we sequenced the genomes of 32 worldwide S. pombe strains and examined the pattern of polymorphisms across their genomes. In addition to introns and untranslated regions (UTRs), intergenic regions also exhibited lower levels of nucleotide diversity than synonymous sites, suggesting that a considerable amount of noncoding DNA is under selective constraint and thus likely to be functional. A number of genomic regions showed a reduction of nucleotide diversity probably caused by selective sweeps. We also identified a region close to the end of chromosome 3 where an extremely high level of divergence was observed between 5 of the 32 strains and the remain 27, possibly due to introgression, strong positive selection, or that region being responsible for reproductive isolation. Our study should serve as an important starting point in using a population genomics approach to further elucidate the biology of this important model organism.

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Two examples of putative partial sweep events on chromosomes 1 and 2.The NJ trees shown on the left are the same as in Figure 1a. The strains in red share long haplotypes. Distributions of the nucleotide diversity around the long haplotypes based on a sliding window of 10 kb with a 2 kb increment are shown on the right. Black and red lines represent the nucleotide diversity of all individuals and the nucleotide diversity of the subsamples sharing the haplotypes, respectively.
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pone-0104241-g006: Two examples of putative partial sweep events on chromosomes 1 and 2.The NJ trees shown on the left are the same as in Figure 1a. The strains in red share long haplotypes. Distributions of the nucleotide diversity around the long haplotypes based on a sliding window of 10 kb with a 2 kb increment are shown on the right. Black and red lines represent the nucleotide diversity of all individuals and the nucleotide diversity of the subsamples sharing the haplotypes, respectively.

Mentions: The signatures of selection may be weak if a sweep has not yet fixed in the species, or if the sweep operates only in a particular geographic region. We explored this possibility by using the pairwise haplotype sharing (PHS) test [25]. This test aims to detect regions where certain individuals share a haplotype over a longer distance than expected, which would indicate a local selective sweep. Indeed, a number of putative partial selective sweep events were identified (see Table S2 for a list of SNPs with the top 0.1% PHS values). Two examples (one on chromosome 1 and the other on chromosome 2) which best illustrate the patterns of polymorphisms expected by partial selective sweeps are shown in Figure 6 (see also Table S4 for lists of protein-coding genes in the two regions). The 2.8–2.9 Mb region of chromosome 1 discussed above also contained several SNPs with high PHS values, although we cannot rule out the possibility that these mutations accumulated in the small number of strains after a complete selective sweep that affected the entire population. In all of the regions showing signatures of partial selective sweeps, the individuals sharing long haplotypes tend to be clustered in the NJ tree, suggesting that in each case the selective sweep was prevented from affecting the entire population. This could be because the sweep started too recently or because differentiation within the population has slowed down the progress of the sweep. Local adaption would be another possible reason for observing a partial sweep.


Population genomics of the fission yeast Schizosaccharomyces pombe.

Fawcett JA, Iida T, Takuno S, Sugino RP, Kado T, Kugou K, Mura S, Kobayashi T, Ohta K, Nakayama J, Innan H - PLoS ONE (2014)

Two examples of putative partial sweep events on chromosomes 1 and 2.The NJ trees shown on the left are the same as in Figure 1a. The strains in red share long haplotypes. Distributions of the nucleotide diversity around the long haplotypes based on a sliding window of 10 kb with a 2 kb increment are shown on the right. Black and red lines represent the nucleotide diversity of all individuals and the nucleotide diversity of the subsamples sharing the haplotypes, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4128662&req=5

pone-0104241-g006: Two examples of putative partial sweep events on chromosomes 1 and 2.The NJ trees shown on the left are the same as in Figure 1a. The strains in red share long haplotypes. Distributions of the nucleotide diversity around the long haplotypes based on a sliding window of 10 kb with a 2 kb increment are shown on the right. Black and red lines represent the nucleotide diversity of all individuals and the nucleotide diversity of the subsamples sharing the haplotypes, respectively.
Mentions: The signatures of selection may be weak if a sweep has not yet fixed in the species, or if the sweep operates only in a particular geographic region. We explored this possibility by using the pairwise haplotype sharing (PHS) test [25]. This test aims to detect regions where certain individuals share a haplotype over a longer distance than expected, which would indicate a local selective sweep. Indeed, a number of putative partial selective sweep events were identified (see Table S2 for a list of SNPs with the top 0.1% PHS values). Two examples (one on chromosome 1 and the other on chromosome 2) which best illustrate the patterns of polymorphisms expected by partial selective sweeps are shown in Figure 6 (see also Table S4 for lists of protein-coding genes in the two regions). The 2.8–2.9 Mb region of chromosome 1 discussed above also contained several SNPs with high PHS values, although we cannot rule out the possibility that these mutations accumulated in the small number of strains after a complete selective sweep that affected the entire population. In all of the regions showing signatures of partial selective sweeps, the individuals sharing long haplotypes tend to be clustered in the NJ tree, suggesting that in each case the selective sweep was prevented from affecting the entire population. This could be because the sweep started too recently or because differentiation within the population has slowed down the progress of the sweep. Local adaption would be another possible reason for observing a partial sweep.

Bottom Line: In addition to introns and untranslated regions (UTRs), intergenic regions also exhibited lower levels of nucleotide diversity than synonymous sites, suggesting that a considerable amount of noncoding DNA is under selective constraint and thus likely to be functional.A number of genomic regions showed a reduction of nucleotide diversity probably caused by selective sweeps.Our study should serve as an important starting point in using a population genomics approach to further elucidate the biology of this important model organism.

View Article: PubMed Central - PubMed

Affiliation: Graduate University for Advanced Studies, Hayama, Kanagawa, Japan.

ABSTRACT
The fission yeast Schizosaccharomyces pombe has been widely used as a model eukaryote to study a diverse range of biological processes. However, population genetic studies of this species have been limited to date, and we know very little about the evolutionary processes and selective pressures that are shaping its genome. Here, we sequenced the genomes of 32 worldwide S. pombe strains and examined the pattern of polymorphisms across their genomes. In addition to introns and untranslated regions (UTRs), intergenic regions also exhibited lower levels of nucleotide diversity than synonymous sites, suggesting that a considerable amount of noncoding DNA is under selective constraint and thus likely to be functional. A number of genomic regions showed a reduction of nucleotide diversity probably caused by selective sweeps. We also identified a region close to the end of chromosome 3 where an extremely high level of divergence was observed between 5 of the 32 strains and the remain 27, possibly due to introgression, strong positive selection, or that region being responsible for reproductive isolation. Our study should serve as an important starting point in using a population genomics approach to further elucidate the biology of this important model organism.

Show MeSH