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Developmental constraints on vertebrate genome evolution.

Roux J, Robinson-Rechavi M - PLoS Genet. (2008)

Bottom Line: We show that, in both species, genes expressed early in development (1) have a more dramatic effect of knock-out or mutation and (2) are more likely to revert to single copy after whole genome duplication, relative to genes expressed late.We determine the pattern of these constraints, which differs from the model used to describe vertebrate morphological conservation ("hourglass" model).While morphological constraints reach a maximum at mid-development (the "phylotypic" stage), genomic constraints appear to decrease in a monotonous manner over developmental time.

View Article: PubMed Central - PubMed

Affiliation: Université de Lausanne, Département d'Ecologie et d'Evolution, Quartier Sorge, Lausanne, Switzerland.

ABSTRACT
Constraints in embryonic development are thought to bias the direction of evolution by making some changes less likely, and others more likely, depending on their consequences on ontogeny. Here, we characterize the constraints acting on genome evolution in vertebrates. We used gene expression data from two vertebrates: zebrafish, using a microarray experiment spanning 14 stages of development, and mouse, using EST counts for 26 stages of development. We show that, in both species, genes expressed early in development (1) have a more dramatic effect of knock-out or mutation and (2) are more likely to revert to single copy after whole genome duplication, relative to genes expressed late. This supports high constraints on early stages of vertebrate development, making them less open to innovations (gene gain or gene loss). Results are robust to different sources of data -- gene expression from microarrays, ESTs, or in situ hybridizations; and mutants from directed KO, transgenic insertions, point mutations, or morpholinos. We determine the pattern of these constraints, which differs from the model used to describe vertebrate morphological conservation ("hourglass" model). While morphological constraints reach a maximum at mid-development (the "phylotypic" stage), genomic constraints appear to decrease in a monotonous manner over developmental time.

Show MeSH
Variation across mouse development of the expression of rapidly evolving genes (25% highest dN/dS) compared to slowly evolving genes (25% lowest dN/dS).Only singletons for 2R were considered. Legend as in Figure 4.
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pgen-1000311-g007: Variation across mouse development of the expression of rapidly evolving genes (25% highest dN/dS) compared to slowly evolving genes (25% lowest dN/dS).Only singletons for 2R were considered. Legend as in Figure 4.

Mentions: In mouse, we considered only singletons after 2R genome duplication, and we compared the slowest evolving genes (25% lower dN/dS) with the fastest evolving genes (25% higher dN/dS). There is a significant correlation with time of expression (Figure 7). Genes with strong sequence constraints (low dN/dS) tend to be expressed early in development.


Developmental constraints on vertebrate genome evolution.

Roux J, Robinson-Rechavi M - PLoS Genet. (2008)

Variation across mouse development of the expression of rapidly evolving genes (25% highest dN/dS) compared to slowly evolving genes (25% lowest dN/dS).Only singletons for 2R were considered. Legend as in Figure 4.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2600815&req=5

pgen-1000311-g007: Variation across mouse development of the expression of rapidly evolving genes (25% highest dN/dS) compared to slowly evolving genes (25% lowest dN/dS).Only singletons for 2R were considered. Legend as in Figure 4.
Mentions: In mouse, we considered only singletons after 2R genome duplication, and we compared the slowest evolving genes (25% lower dN/dS) with the fastest evolving genes (25% higher dN/dS). There is a significant correlation with time of expression (Figure 7). Genes with strong sequence constraints (low dN/dS) tend to be expressed early in development.

Bottom Line: We show that, in both species, genes expressed early in development (1) have a more dramatic effect of knock-out or mutation and (2) are more likely to revert to single copy after whole genome duplication, relative to genes expressed late.We determine the pattern of these constraints, which differs from the model used to describe vertebrate morphological conservation ("hourglass" model).While morphological constraints reach a maximum at mid-development (the "phylotypic" stage), genomic constraints appear to decrease in a monotonous manner over developmental time.

View Article: PubMed Central - PubMed

Affiliation: Université de Lausanne, Département d'Ecologie et d'Evolution, Quartier Sorge, Lausanne, Switzerland.

ABSTRACT
Constraints in embryonic development are thought to bias the direction of evolution by making some changes less likely, and others more likely, depending on their consequences on ontogeny. Here, we characterize the constraints acting on genome evolution in vertebrates. We used gene expression data from two vertebrates: zebrafish, using a microarray experiment spanning 14 stages of development, and mouse, using EST counts for 26 stages of development. We show that, in both species, genes expressed early in development (1) have a more dramatic effect of knock-out or mutation and (2) are more likely to revert to single copy after whole genome duplication, relative to genes expressed late. This supports high constraints on early stages of vertebrate development, making them less open to innovations (gene gain or gene loss). Results are robust to different sources of data -- gene expression from microarrays, ESTs, or in situ hybridizations; and mutants from directed KO, transgenic insertions, point mutations, or morpholinos. We determine the pattern of these constraints, which differs from the model used to describe vertebrate morphological conservation ("hourglass" model). While morphological constraints reach a maximum at mid-development (the "phylotypic" stage), genomic constraints appear to decrease in a monotonous manner over developmental time.

Show MeSH