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G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae.

Capra JA, Paeschke K, Singh M, Zakian VA - PLoS Comput. Biol. (2010)

Bottom Line: We found that G4 DNA motifs were significantly more conserved than expected by chance, and the nucleotide-level conservation patterns suggested that the motif conservation was the result of the formation of G4 DNA structures.We also performed the first analysis of G4 DNA motifs in the mitochondria, and surprisingly found a tenfold higher concentration of the motifs in the AT-rich yeast mitochondrial DNA than in nuclear DNA.The evolutionary conservation of the G4 DNA motif and its association with specific genome features supports the hypothesis that G4 DNA has in vivo functions that are under evolutionary constraint.

View Article: PubMed Central - PubMed

Affiliation: Department of Computer Science, Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USA.

ABSTRACT
G-quadruplex DNA is a four-stranded DNA structure formed by non-Watson-Crick base pairing between stacked sets of four guanines. Many possible functions have been proposed for this structure, but its in vivo role in the cell is still largely unresolved. We carried out a genome-wide survey of the evolutionary conservation of regions with the potential to form G-quadruplex DNA structures (G4 DNA motifs) across seven yeast species. We found that G4 DNA motifs were significantly more conserved than expected by chance, and the nucleotide-level conservation patterns suggested that the motif conservation was the result of the formation of G4 DNA structures. We characterized the association of conserved and non-conserved G4 DNA motifs in Saccharomyces cerevisiae with more than 40 known genome features and gene classes. Our comprehensive, integrated evolutionary and functional analysis confirmed the previously observed associations of G4 DNA motifs with promoter regions and the rDNA, and it identified several previously unrecognized associations of G4 DNA motifs with genomic features, such as mitotic and meiotic double-strand break sites (DSBs). Conserved G4 DNA motifs maintained strong associations with promoters and the rDNA, but not with DSBs. We also performed the first analysis of G4 DNA motifs in the mitochondria, and surprisingly found a tenfold higher concentration of the motifs in the AT-rich yeast mitochondrial DNA than in nuclear DNA. The evolutionary conservation of the G4 DNA motif and its association with specific genome features supports the hypothesis that G4 DNA has in vivo functions that are under evolutionary constraint.

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The evolutionary conservation of G4 DNA motifs between S. cerevisiae and six related yeast species.(A) The phylogenetic tree for the seven yeast species considered in this study (not to scale). The four sensu stricto species (S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) diverged from S. cerevisiae within the last ∼20 million years. S. castelli and S. kluyveri are considerably more distant [21]. The percent sequence identity to S. cerevisiae over the alignable regions is given in parentheses. (B) The evolutionary conservation of the 507 non-telomeric, nuclear S. cerevisiae G4 DNA motifs in sequence regions that could be aligned to at least one other genome. Significantly more G4 DNA motifs were conserved than expected by chance between S. cerevisiae and five of the six species considered. The one exception was S. kluyveri, which is the most distant and GC-rich species among the seven yeasts.
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pcbi-1000861-g002: The evolutionary conservation of G4 DNA motifs between S. cerevisiae and six related yeast species.(A) The phylogenetic tree for the seven yeast species considered in this study (not to scale). The four sensu stricto species (S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) diverged from S. cerevisiae within the last ∼20 million years. S. castelli and S. kluyveri are considerably more distant [21]. The percent sequence identity to S. cerevisiae over the alignable regions is given in parentheses. (B) The evolutionary conservation of the 507 non-telomeric, nuclear S. cerevisiae G4 DNA motifs in sequence regions that could be aligned to at least one other genome. Significantly more G4 DNA motifs were conserved than expected by chance between S. cerevisiae and five of the six species considered. The one exception was S. kluyveri, which is the most distant and GC-rich species among the seven yeasts.

Mentions: We analyzed the sequence conservation of S. cerevisiae G4 DNA motifs across the genomes of seven Saccharomyces strains (Fig. 2A). The five sensu stricto strains (S. cerevisiae, S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) are estimated to have diverged from each other ∼10–20 million years ago, while S. castellii and S. kluyveri are more evolutionarily distant from S. cerevisiae (∼100 million years since divergence) [21]. The overall number of G4 DNA motifs found in each of these species was within a factor of two of the number found in S. cerevisiae (Table 1).


G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae.

Capra JA, Paeschke K, Singh M, Zakian VA - PLoS Comput. Biol. (2010)

The evolutionary conservation of G4 DNA motifs between S. cerevisiae and six related yeast species.(A) The phylogenetic tree for the seven yeast species considered in this study (not to scale). The four sensu stricto species (S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) diverged from S. cerevisiae within the last ∼20 million years. S. castelli and S. kluyveri are considerably more distant [21]. The percent sequence identity to S. cerevisiae over the alignable regions is given in parentheses. (B) The evolutionary conservation of the 507 non-telomeric, nuclear S. cerevisiae G4 DNA motifs in sequence regions that could be aligned to at least one other genome. Significantly more G4 DNA motifs were conserved than expected by chance between S. cerevisiae and five of the six species considered. The one exception was S. kluyveri, which is the most distant and GC-rich species among the seven yeasts.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2908698&req=5

pcbi-1000861-g002: The evolutionary conservation of G4 DNA motifs between S. cerevisiae and six related yeast species.(A) The phylogenetic tree for the seven yeast species considered in this study (not to scale). The four sensu stricto species (S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) diverged from S. cerevisiae within the last ∼20 million years. S. castelli and S. kluyveri are considerably more distant [21]. The percent sequence identity to S. cerevisiae over the alignable regions is given in parentheses. (B) The evolutionary conservation of the 507 non-telomeric, nuclear S. cerevisiae G4 DNA motifs in sequence regions that could be aligned to at least one other genome. Significantly more G4 DNA motifs were conserved than expected by chance between S. cerevisiae and five of the six species considered. The one exception was S. kluyveri, which is the most distant and GC-rich species among the seven yeasts.
Mentions: We analyzed the sequence conservation of S. cerevisiae G4 DNA motifs across the genomes of seven Saccharomyces strains (Fig. 2A). The five sensu stricto strains (S. cerevisiae, S. paradoxus, S. mikatae, S. kudriavzevii, S. bayanus) are estimated to have diverged from each other ∼10–20 million years ago, while S. castellii and S. kluyveri are more evolutionarily distant from S. cerevisiae (∼100 million years since divergence) [21]. The overall number of G4 DNA motifs found in each of these species was within a factor of two of the number found in S. cerevisiae (Table 1).

Bottom Line: We found that G4 DNA motifs were significantly more conserved than expected by chance, and the nucleotide-level conservation patterns suggested that the motif conservation was the result of the formation of G4 DNA structures.We also performed the first analysis of G4 DNA motifs in the mitochondria, and surprisingly found a tenfold higher concentration of the motifs in the AT-rich yeast mitochondrial DNA than in nuclear DNA.The evolutionary conservation of the G4 DNA motif and its association with specific genome features supports the hypothesis that G4 DNA has in vivo functions that are under evolutionary constraint.

View Article: PubMed Central - PubMed

Affiliation: Department of Computer Science, Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USA.

ABSTRACT
G-quadruplex DNA is a four-stranded DNA structure formed by non-Watson-Crick base pairing between stacked sets of four guanines. Many possible functions have been proposed for this structure, but its in vivo role in the cell is still largely unresolved. We carried out a genome-wide survey of the evolutionary conservation of regions with the potential to form G-quadruplex DNA structures (G4 DNA motifs) across seven yeast species. We found that G4 DNA motifs were significantly more conserved than expected by chance, and the nucleotide-level conservation patterns suggested that the motif conservation was the result of the formation of G4 DNA structures. We characterized the association of conserved and non-conserved G4 DNA motifs in Saccharomyces cerevisiae with more than 40 known genome features and gene classes. Our comprehensive, integrated evolutionary and functional analysis confirmed the previously observed associations of G4 DNA motifs with promoter regions and the rDNA, and it identified several previously unrecognized associations of G4 DNA motifs with genomic features, such as mitotic and meiotic double-strand break sites (DSBs). Conserved G4 DNA motifs maintained strong associations with promoters and the rDNA, but not with DSBs. We also performed the first analysis of G4 DNA motifs in the mitochondria, and surprisingly found a tenfold higher concentration of the motifs in the AT-rich yeast mitochondrial DNA than in nuclear DNA. The evolutionary conservation of the G4 DNA motif and its association with specific genome features supports the hypothesis that G4 DNA has in vivo functions that are under evolutionary constraint.

Show MeSH