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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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Genome-wide distribution of nucleotide diversity  and Tajima's D.The values were calculated for each sliding window of 20 kb with an increment of 4 kb. The putative selective sweep region on chromosome 1 with low nucleotide diversity and low Tajima's D is indicated by a blue downward triangle. The mating locus region on chromosome 2 and another region on chromosome 3 showing high nucleotide diversity are indicated by red downward triangles. The gray shaded regions correspond to centromeric regions.
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pone-0104241-g005: Genome-wide distribution of nucleotide diversity and Tajima's D.The values were calculated for each sliding window of 20 kb with an increment of 4 kb. The putative selective sweep region on chromosome 1 with low nucleotide diversity and low Tajima's D is indicated by a blue downward triangle. The mating locus region on chromosome 2 and another region on chromosome 3 showing high nucleotide diversity are indicated by red downward triangles. The gray shaded regions correspond to centromeric regions.

Mentions: We then applied a sliding window analysis of 20 kb with an increment of 4 kb to each chromosome. Provided the estimated degree of linkage, this window size should be reasonable to obtain a rough picture of the large-scale variation of nucleotide diversity across the genome. A large region with reduced polymorphism is a signature of a recent selective sweep, while an exceptionally high level of nucleotide diversity might indicate some other form of selection. As shown in Figure 5, the S. pombe genome exhibits little evidence of a selective sweep caused by the recent fixation of an adaptive mutation. One exception is found in the middle of chromosome 1 (around 2.8–2.9 Mb), which displays a long stretch of low nucleotide diversity and negative Tajima's D. However, it is interesting to note that this region does contain a certain amount of nucleotide diversity, even though a very recent sweep would typically create a large region with almost no genetic variation. One possibility is that the sweep event was not very recent and that mutations have accumulated after the sweep. On the other hand, careful inspection of this region shows that most of the minor alleles at the polymorphic sites (many of which are singletons) are concentrated in 4 strains, including 3 (CBS10391 (#1), CBS2628 (#2) and CBS 10394 (#9); the fourth one is CBS10468 (#22)) that are amongst the earliest diverging strains according to the NJ tree shown in Figure 1 (see also Table S2). In addition, the remaining strains share an unexpectedly long haplotype (see below). Thus, an alternative possibility would be that the sweep is incomplete and has not yet reached fixation. A list of protein-coding genes in this region is provided in Table S3.


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)

Genome-wide distribution of nucleotide diversity  and Tajima's D.The values were calculated for each sliding window of 20 kb with an increment of 4 kb. The putative selective sweep region on chromosome 1 with low nucleotide diversity and low Tajima's D is indicated by a blue downward triangle. The mating locus region on chromosome 2 and another region on chromosome 3 showing high nucleotide diversity are indicated by red downward triangles. The gray shaded regions correspond to centromeric regions.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0104241-g005: Genome-wide distribution of nucleotide diversity and Tajima's D.The values were calculated for each sliding window of 20 kb with an increment of 4 kb. The putative selective sweep region on chromosome 1 with low nucleotide diversity and low Tajima's D is indicated by a blue downward triangle. The mating locus region on chromosome 2 and another region on chromosome 3 showing high nucleotide diversity are indicated by red downward triangles. The gray shaded regions correspond to centromeric regions.
Mentions: We then applied a sliding window analysis of 20 kb with an increment of 4 kb to each chromosome. Provided the estimated degree of linkage, this window size should be reasonable to obtain a rough picture of the large-scale variation of nucleotide diversity across the genome. A large region with reduced polymorphism is a signature of a recent selective sweep, while an exceptionally high level of nucleotide diversity might indicate some other form of selection. As shown in Figure 5, the S. pombe genome exhibits little evidence of a selective sweep caused by the recent fixation of an adaptive mutation. One exception is found in the middle of chromosome 1 (around 2.8–2.9 Mb), which displays a long stretch of low nucleotide diversity and negative Tajima's D. However, it is interesting to note that this region does contain a certain amount of nucleotide diversity, even though a very recent sweep would typically create a large region with almost no genetic variation. One possibility is that the sweep event was not very recent and that mutations have accumulated after the sweep. On the other hand, careful inspection of this region shows that most of the minor alleles at the polymorphic sites (many of which are singletons) are concentrated in 4 strains, including 3 (CBS10391 (#1), CBS2628 (#2) and CBS 10394 (#9); the fourth one is CBS10468 (#22)) that are amongst the earliest diverging strains according to the NJ tree shown in Figure 1 (see also Table S2). In addition, the remaining strains share an unexpectedly long haplotype (see below). Thus, an alternative possibility would be that the sweep is incomplete and has not yet reached fixation. A list of protein-coding genes in this region is provided in Table S3.

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