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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 its standard deviation (GCσ).Each domain GC content and GCσ are represented by a point on 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-g008: A two dimensional joint distribution of homogeneous domain GC content and its standard deviation (GCσ).Each domain GC content and GCσ are represented by a point on 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: To further study the GC content fluctuations within compositional domains, we looked at their compositional variability. Compositional variability is measured from the standard deviation (GCσ) of the GC content of each domain calculated over short nonoverlapping windows within the domain (see Materials and Methods). Figure 8 presents two-dimensional joint distribution of homogeneous domain GC content and GCσ. Interestingly, the GCσ values of most mammalian domains are narrowly distributed around 11% GCσ and, with the exception of opossum that exhibits a smaller variation. In other words, GC-rich domains are more erratic in their composition (high GCσ) than GC-poor domains (low GCσ). The high compositional variability of horse and dog is also reflected in the wide range of GCσ values compared with those of the Cetartiodactyla species.


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 its standard deviation (GCσ).Each domain GC content and GCσ are represented by a point on 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-g008: A two dimensional joint distribution of homogeneous domain GC content and its standard deviation (GCσ).Each domain GC content and GCσ are represented by a point on 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: To further study the GC content fluctuations within compositional domains, we looked at their compositional variability. Compositional variability is measured from the standard deviation (GCσ) of the GC content of each domain calculated over short nonoverlapping windows within the domain (see Materials and Methods). Figure 8 presents two-dimensional joint distribution of homogeneous domain GC content and GCσ. Interestingly, the GCσ values of most mammalian domains are narrowly distributed around 11% GCσ and, with the exception of opossum that exhibits a smaller variation. In other words, GC-rich domains are more erratic in their composition (high GCσ) than GC-poor domains (low GCσ). The high compositional variability of horse and dog is also reflected in the wide range of GCσ values compared with those of the Cetartiodactyla species.

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