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Evidence for a common evolutionary rate in metazoan transcriptional networks.

Carvunis AR, Wang T, Skola D, Yu A, Chen J, Kreisberg JF, Ideker T - Elife (2015)

Bottom Line: Here, we show that these conflicting interpretations resulted from differing methodologies.Strikingly, we found that transcriptional networks evolve at a common rate across the three animal lineages.Furthermore, differences in rates of genome divergence were greatly reduced when restricting comparisons to chromatin-accessible sequences.

View Article: PubMed Central - PubMed

Affiliation: Department of Medicine, University of California, San Diego, La Jolla, United States.

ABSTRACT
Genome sequences diverge more rapidly in mammals than in other animal lineages, such as birds or insects. However, the effect of this rapid divergence on transcriptional evolution remains unclear. Recent reports have indicated a faster divergence of transcription factor binding in mammals than in insects, but others found the reverse for mRNA expression. Here, we show that these conflicting interpretations resulted from differing methodologies. We performed an integrated analysis of transcriptional network evolution by examining mRNA expression, transcription factor binding and cis-regulatory motifs across >25 animal species, including mammals, birds and insects. Strikingly, we found that transcriptional networks evolve at a common rate across the three animal lineages. Furthermore, differences in rates of genome divergence were greatly reduced when restricting comparisons to chromatin-accessible sequences. The evolution of transcription is thus decoupled from the global rate of genome sequence evolution, suggesting that a small fraction of the genome regulates transcription.

No MeSH data available.


Retention of genomic segments is robust to changes in sampled region size and sequence identity threshold.(a) Following the same procedure as in Figure 2 but varying the segment length to 150 bp and (b) increasing the LiftOver minMatch parameter to 0.5.DOI:http://dx.doi.org/10.7554/eLife.11615.008
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fig2s2: Retention of genomic segments is robust to changes in sampled region size and sequence identity threshold.(a) Following the same procedure as in Figure 2 but varying the segment length to 150 bp and (b) increasing the LiftOver minMatch parameter to 0.5.DOI:http://dx.doi.org/10.7554/eLife.11615.008

Mentions: As a baseline, we first performed a comparative analysis of the evolution of genome sequences. We randomly sampled genomic segments from designated reference genomes: Mus musculus domesticus (C57BL/6) for mammals, Gallus gallus for birds and Drosophila melanogaster for insects. The rates at which genomic segments that retained homologs with the other species within each lineage accumulate nucleotide substitutions were then estimated and compared using our statistical framework. Segments retaining homologs displayed high sequence conservation across all three lineages, although our framework detected a slightly but significantly faster divergence in insects than in mammals or birds (P<0.05; Figure 2—figure supplement 1). Next, we compared the rates at which randomly sampled genomic segments lost homology with the other species within each lineage. We observed a much larger difference in evolutionary rates across lineages using this measure (P<0.05; Figure 2; Figure 2—figure supplement 2). For instance, after 100 million years (Myrs) of evolution, only ~30% of mammalian segments retained homology, whereas >60% of bird and insect segments did. These findings recapitulated previous observations according to which genome sequences are less constrained in mammals than in insects (Siepel et al., 2005) or birds (Zhang et al., 2014).10.7554/eLife.11615.003Figure 1.Statistical framework to evaluate differences in evolutionary rates of change.


Evidence for a common evolutionary rate in metazoan transcriptional networks.

Carvunis AR, Wang T, Skola D, Yu A, Chen J, Kreisberg JF, Ideker T - Elife (2015)

Retention of genomic segments is robust to changes in sampled region size and sequence identity threshold.(a) Following the same procedure as in Figure 2 but varying the segment length to 150 bp and (b) increasing the LiftOver minMatch parameter to 0.5.DOI:http://dx.doi.org/10.7554/eLife.11615.008
© Copyright Policy
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4764585&req=5

fig2s2: Retention of genomic segments is robust to changes in sampled region size and sequence identity threshold.(a) Following the same procedure as in Figure 2 but varying the segment length to 150 bp and (b) increasing the LiftOver minMatch parameter to 0.5.DOI:http://dx.doi.org/10.7554/eLife.11615.008
Mentions: As a baseline, we first performed a comparative analysis of the evolution of genome sequences. We randomly sampled genomic segments from designated reference genomes: Mus musculus domesticus (C57BL/6) for mammals, Gallus gallus for birds and Drosophila melanogaster for insects. The rates at which genomic segments that retained homologs with the other species within each lineage accumulate nucleotide substitutions were then estimated and compared using our statistical framework. Segments retaining homologs displayed high sequence conservation across all three lineages, although our framework detected a slightly but significantly faster divergence in insects than in mammals or birds (P<0.05; Figure 2—figure supplement 1). Next, we compared the rates at which randomly sampled genomic segments lost homology with the other species within each lineage. We observed a much larger difference in evolutionary rates across lineages using this measure (P<0.05; Figure 2; Figure 2—figure supplement 2). For instance, after 100 million years (Myrs) of evolution, only ~30% of mammalian segments retained homology, whereas >60% of bird and insect segments did. These findings recapitulated previous observations according to which genome sequences are less constrained in mammals than in insects (Siepel et al., 2005) or birds (Zhang et al., 2014).10.7554/eLife.11615.003Figure 1.Statistical framework to evaluate differences in evolutionary rates of change.

Bottom Line: Here, we show that these conflicting interpretations resulted from differing methodologies.Strikingly, we found that transcriptional networks evolve at a common rate across the three animal lineages.Furthermore, differences in rates of genome divergence were greatly reduced when restricting comparisons to chromatin-accessible sequences.

View Article: PubMed Central - PubMed

Affiliation: Department of Medicine, University of California, San Diego, La Jolla, United States.

ABSTRACT
Genome sequences diverge more rapidly in mammals than in other animal lineages, such as birds or insects. However, the effect of this rapid divergence on transcriptional evolution remains unclear. Recent reports have indicated a faster divergence of transcription factor binding in mammals than in insects, but others found the reverse for mRNA expression. Here, we show that these conflicting interpretations resulted from differing methodologies. We performed an integrated analysis of transcriptional network evolution by examining mRNA expression, transcription factor binding and cis-regulatory motifs across >25 animal species, including mammals, birds and insects. Strikingly, we found that transcriptional networks evolve at a common rate across the three animal lineages. Furthermore, differences in rates of genome divergence were greatly reduced when restricting comparisons to chromatin-accessible sequences. The evolution of transcription is thus decoupled from the global rate of genome sequence evolution, suggesting that a small fraction of the genome regulates transcription.

No MeSH data available.