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A comparative study and a phylogenetic exploration of the compositional architectures of mammalian nuclear genomes.

Elhaik E, Graur D - PLoS Comput. Biol. (2014)

Bottom Line: If invalid, the murid genome compositional organization would be closer to an ancestral state.We demonstrate that the compositional organization of the murid genome differs from those of primates and laurasiatherians, a phenomenon previously termed the "murid shift," and in many ways resembles the genome of opossum.We find no support to the "isochore theory." Instead, our findings depict the mammalian genome as a tapestry of mostly short homogeneous and nonhomogeneous domains and few long ones thus providing strong evidence in favor of the compositional domain model and seem to invalidate clade Euarchontoglires.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.

ABSTRACT
For the past four decades the compositional organization of the mammalian genome posed a formidable challenge to molecular evolutionists attempting to explain it from an evolutionary perspective. Unfortunately, most of the explanations adhered to the "isochore theory," which has long been rebutted. Recently, an alternative compositional domain model was proposed depicting the human and cow genomes as composed mostly of short compositionally homogeneous and nonhomogeneous domains and a few long ones. We test the validity of this model through a rigorous sequence-based analysis of eleven completely sequenced mammalian and avian genomes. Seven attributes of compositional domains are used in the analyses: (1) the number of compositional domains, (2) compositional domain-length distribution, (3) density of compositional domains, (4) genome coverage by the different domain types, (5) degree of fit to a power-law distribution, (6) compositional domain GC content, and (7) the joint distribution of GC content and length of the different domain types. We discuss the evolution of these attributes in light of two competing phylogenetic hypotheses that differ from each other in the validity of clade Euarchontoglires. If valid, the murid genome compositional organization would be a derived state and exhibit a high similarity to that of other mammals. If invalid, the murid genome compositional organization would be closer to an ancestral state. We demonstrate that the compositional organization of the murid genome differs from those of primates and laurasiatherians, a phenomenon previously termed the "murid shift," and in many ways resembles the genome of opossum. We find no support to the "isochore theory." Instead, our findings depict the mammalian genome as a tapestry of mostly short homogeneous and nonhomogeneous domains and few long ones thus providing strong evidence in favor of the compositional domain model and seem to invalidate clade Euarchontoglires.

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A two dimensional joint distribution of homogeneous domain GC content and length in a log scale.Each domain's GC content and length are represented by a point in the map. The frequency of different points is represented by colors ranging from red (highest frequency) to blue (lowest frequency). The mean GC content of the mammalian genome is marked by horizontal line.
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pcbi-1003925-g009: A two dimensional joint distribution of homogeneous domain GC content and length in a log scale.Each domain's GC content and length are represented by a point in the map. The frequency of different points is represented by colors ranging from red (highest frequency) to blue (lowest frequency). The mean GC content of the mammalian genome is marked by horizontal line.

Mentions: The two-dimensional joint distributions of homogeneous domain GC content and length are shown in Figure 9. These measures are not correlated (r = ∼0). As shown before, the majority of domains in all genomes are short (6–8 kb), and their GC content distributes close to the mammalian genome mean GC content. With the exception of murids, homogeneous domains are significantly more AT-rich than nonhomogeneous domains (Kolmogorov-Smirnov goodness-of-fit test, p<0.01). The genomic landscape topologies of primates, laurasiatherian, and murids are remarkably similar with short (103–104 bp) GC-rich domains 1.3–1.7 times more frequent than GC-poor domains and medium-large (105–106 bp) GC-rich domains 1–2 times more frequent than GC-poor domains (Table S2). This ratio is opposite for both domain size groups (0.7 and 0.32, respectively) in opossum, which implies a major domain fusion process that affected the tetrapod genome.


A comparative study and a phylogenetic exploration of the compositional architectures of mammalian nuclear genomes.

Elhaik E, Graur D - PLoS Comput. Biol. (2014)

A two dimensional joint distribution of homogeneous domain GC content and length in a log scale.Each domain's GC content and length are represented by a point in the map. The frequency of different points is represented by colors ranging from red (highest frequency) to blue (lowest frequency). The mean GC content of the mammalian genome is marked by horizontal line.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4222635&req=5

pcbi-1003925-g009: A two dimensional joint distribution of homogeneous domain GC content and length in a log scale.Each domain's GC content and length are represented by a point in the map. The frequency of different points is represented by colors ranging from red (highest frequency) to blue (lowest frequency). The mean GC content of the mammalian genome is marked by horizontal line.
Mentions: The two-dimensional joint distributions of homogeneous domain GC content and length are shown in Figure 9. These measures are not correlated (r = ∼0). As shown before, the majority of domains in all genomes are short (6–8 kb), and their GC content distributes close to the mammalian genome mean GC content. With the exception of murids, homogeneous domains are significantly more AT-rich than nonhomogeneous domains (Kolmogorov-Smirnov goodness-of-fit test, p<0.01). The genomic landscape topologies of primates, laurasiatherian, and murids are remarkably similar with short (103–104 bp) GC-rich domains 1.3–1.7 times more frequent than GC-poor domains and medium-large (105–106 bp) GC-rich domains 1–2 times more frequent than GC-poor domains (Table S2). This ratio is opposite for both domain size groups (0.7 and 0.32, respectively) in opossum, which implies a major domain fusion process that affected the tetrapod genome.

Bottom Line: If invalid, the murid genome compositional organization would be closer to an ancestral state.We demonstrate that the compositional organization of the murid genome differs from those of primates and laurasiatherians, a phenomenon previously termed the "murid shift," and in many ways resembles the genome of opossum.We find no support to the "isochore theory." Instead, our findings depict the mammalian genome as a tapestry of mostly short homogeneous and nonhomogeneous domains and few long ones thus providing strong evidence in favor of the compositional domain model and seem to invalidate clade Euarchontoglires.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.

ABSTRACT
For the past four decades the compositional organization of the mammalian genome posed a formidable challenge to molecular evolutionists attempting to explain it from an evolutionary perspective. Unfortunately, most of the explanations adhered to the "isochore theory," which has long been rebutted. Recently, an alternative compositional domain model was proposed depicting the human and cow genomes as composed mostly of short compositionally homogeneous and nonhomogeneous domains and a few long ones. We test the validity of this model through a rigorous sequence-based analysis of eleven completely sequenced mammalian and avian genomes. Seven attributes of compositional domains are used in the analyses: (1) the number of compositional domains, (2) compositional domain-length distribution, (3) density of compositional domains, (4) genome coverage by the different domain types, (5) degree of fit to a power-law distribution, (6) compositional domain GC content, and (7) the joint distribution of GC content and length of the different domain types. We discuss the evolution of these attributes in light of two competing phylogenetic hypotheses that differ from each other in the validity of clade Euarchontoglires. If valid, the murid genome compositional organization would be a derived state and exhibit a high similarity to that of other mammals. If invalid, the murid genome compositional organization would be closer to an ancestral state. We demonstrate that the compositional organization of the murid genome differs from those of primates and laurasiatherians, a phenomenon previously termed the "murid shift," and in many ways resembles the genome of opossum. We find no support to the "isochore theory." Instead, our findings depict the mammalian genome as a tapestry of mostly short homogeneous and nonhomogeneous domains and few long ones thus providing strong evidence in favor of the compositional domain model and seem to invalidate clade Euarchontoglires.

Show MeSH