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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 ratio of expressed orthologs of zebrafish singletons after the fish specific genome duplication (FSGD) relative to orthologs of zebrafish duplicates.Legend as in Figure 4.
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pgen-1000311-g006: Variation across mouse development of the ratio of expressed orthologs of zebrafish singletons after the fish specific genome duplication (FSGD) relative to orthologs of zebrafish duplicates.Legend as in Figure 4.

Mentions: Two scenarios can explain this result. First, retention of two copies may be more likely after the whole genome duplication for genes less expressed in early development. Second, the retention of genes may be unbiased relative to development, but duplicate genes may evolve secondarily lower expression in early development. To get a proxy of the ancestral state before whole genome duplication, we used again mouse data, which has diverged from zebrafish before the fish specific duplication. We compared mouse orthologs of zebrafish duplicates to mouse orthologs of zebrafish singletons, regarding their expression in development (Figure 6). Mouse orthologs of duplicates are significantly less expressed in early development compared to orthologs of singletons. This result in mouse is consistent with the observations in zebrafish, and the most parsimonious explanation is that expression was similar in the ancestor of the two lineages. Therefore we can accept the first hypothesis: after the fish specific whole genome duplication, there was preferential retention of duplicates less expressed in early development.


Developmental constraints on vertebrate genome evolution.

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

Variation across mouse development of the ratio of expressed orthologs of zebrafish singletons after the fish specific genome duplication (FSGD) relative to orthologs of zebrafish duplicates.Legend as in Figure 4.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000311-g006: Variation across mouse development of the ratio of expressed orthologs of zebrafish singletons after the fish specific genome duplication (FSGD) relative to orthologs of zebrafish duplicates.Legend as in Figure 4.
Mentions: Two scenarios can explain this result. First, retention of two copies may be more likely after the whole genome duplication for genes less expressed in early development. Second, the retention of genes may be unbiased relative to development, but duplicate genes may evolve secondarily lower expression in early development. To get a proxy of the ancestral state before whole genome duplication, we used again mouse data, which has diverged from zebrafish before the fish specific duplication. We compared mouse orthologs of zebrafish duplicates to mouse orthologs of zebrafish singletons, regarding their expression in development (Figure 6). Mouse orthologs of duplicates are significantly less expressed in early development compared to orthologs of singletons. This result in mouse is consistent with the observations in zebrafish, and the most parsimonious explanation is that expression was similar in the ancestor of the two lineages. Therefore we can accept the first hypothesis: after the fish specific whole genome duplication, there was preferential retention of duplicates less expressed in early 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