Limits...
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
Expression in zebrafish development of genes according to retention after the fish specific whole genome duplication.Median expression profiles of zebrafish duplicates from the fish specific whole genome duplication in red dashed line and triangles, and of singletons in black solid line and circles. Legend as in Figure 2.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2600815&req=5

pgen-1000311-g005: Expression in zebrafish development of genes according to retention after the fish specific whole genome duplication.Median expression profiles of zebrafish duplicates from the fish specific whole genome duplication in red dashed line and triangles, and of singletons in black solid line and circles. Legend as in Figure 2.

Mentions: The fish specific whole genome duplication [19] provides us with a natural experiment on constraints on gene doubling: after this event approximately 85% of duplicated genes lost one copy, and the subset which retained both copies is known to be biased relative to function and selective pressure [20]. Thus we tested if duplicate gene expression pattern in zebrafish development was biased compared to singletons. We plotted the median expression profiles of duplicates originating from the fish specific whole genome duplication, and of singletons, genes whose duplicate copy has been lost after the genome duplication (Figure 5). Duplicates are less expressed in early stages of development. The difference of median expression decreases progressively, similar to the observations for essential or abnormal phenotype genes. Larval time points show a maximum expression of duplicates relative to singletons.


Developmental constraints on vertebrate genome evolution.

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

Expression in zebrafish development of genes according to retention after the fish specific whole genome duplication.Median expression profiles of zebrafish duplicates from the fish specific whole genome duplication in red dashed line and triangles, and of singletons in black solid line and circles. Legend as in Figure 2.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000311-g005: Expression in zebrafish development of genes according to retention after the fish specific whole genome duplication.Median expression profiles of zebrafish duplicates from the fish specific whole genome duplication in red dashed line and triangles, and of singletons in black solid line and circles. Legend as in Figure 2.
Mentions: The fish specific whole genome duplication [19] provides us with a natural experiment on constraints on gene doubling: after this event approximately 85% of duplicated genes lost one copy, and the subset which retained both copies is known to be biased relative to function and selective pressure [20]. Thus we tested if duplicate gene expression pattern in zebrafish development was biased compared to singletons. We plotted the median expression profiles of duplicates originating from the fish specific whole genome duplication, and of singletons, genes whose duplicate copy has been lost after the genome duplication (Figure 5). Duplicates are less expressed in early stages of development. The difference of median expression decreases progressively, similar to the observations for essential or abnormal phenotype genes. Larval time points show a maximum expression of duplicates relative to singletons.

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