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Punctuated emergences of genetic and phenotypic innovations in eumetazoan, bilaterian, euteleostome, and hominidae ancestors.

Wenger Y, Galliot B - Genome Biol Evol (2013)

Bottom Line: Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later.For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands).The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics and Evolution, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Geneva, Switzerland.

ABSTRACT
Phenotypic traits derive from the selective recruitment of genetic materials over macroevolutionary times, and protein-coding genes constitute an essential component of these materials. We took advantage of the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. Comparing the proteomes of 23 eukaryotes, we find that 33% human proteins have an ortholog in nonmetazoan species. This premetazoan proteome associates with 43% of all annotated human biological processes. Subsequently, four major waves of innovations can be inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi (bony vertebrates), and hominidae, largely specific to each epoch, whereas early branching deuterostome and chordate phyla show very few innovations. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

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Versatility of novel eumetazoan proteins: Heatmap showing a limited overlap between the protein contents of the BPs that are enriched in novel cnidarian human orthologs.
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evt142-F7: Versatility of novel eumetazoan proteins: Heatmap showing a limited overlap between the protein contents of the BPs that are enriched in novel cnidarian human orthologs.

Mentions: To test whether these eumetazoan-specific novel huBPs correspond to unique genetic sets or rather involve proteins that participate in several phenotypes, we performed an overlap analysis of the protein-enriched BPs that were significant. We found a high variability in the protein overlaps depending on the huBPs combinations considered (fig. 7): few huBP combinations exhibit almost complete overlaps (shown in red), whereas most groups show a limited overlap, in a range from 0% to 50%, illustrating the fact that a subset of proteins may participate in multiple BPs. As a consequence, we assume that proteins related to huBPs that are not expressed in cnidarians yet are nevertheless constrained by their participation in other BPs.Fig. 7.—


Punctuated emergences of genetic and phenotypic innovations in eumetazoan, bilaterian, euteleostome, and hominidae ancestors.

Wenger Y, Galliot B - Genome Biol Evol (2013)

Versatility of novel eumetazoan proteins: Heatmap showing a limited overlap between the protein contents of the BPs that are enriched in novel cnidarian human orthologs.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814200&req=5

evt142-F7: Versatility of novel eumetazoan proteins: Heatmap showing a limited overlap between the protein contents of the BPs that are enriched in novel cnidarian human orthologs.
Mentions: To test whether these eumetazoan-specific novel huBPs correspond to unique genetic sets or rather involve proteins that participate in several phenotypes, we performed an overlap analysis of the protein-enriched BPs that were significant. We found a high variability in the protein overlaps depending on the huBPs combinations considered (fig. 7): few huBP combinations exhibit almost complete overlaps (shown in red), whereas most groups show a limited overlap, in a range from 0% to 50%, illustrating the fact that a subset of proteins may participate in multiple BPs. As a consequence, we assume that proteins related to huBPs that are not expressed in cnidarians yet are nevertheless constrained by their participation in other BPs.Fig. 7.—

Bottom Line: Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later.For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands).The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics and Evolution, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Geneva, Switzerland.

ABSTRACT
Phenotypic traits derive from the selective recruitment of genetic materials over macroevolutionary times, and protein-coding genes constitute an essential component of these materials. We took advantage of the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. Comparing the proteomes of 23 eukaryotes, we find that 33% human proteins have an ortholog in nonmetazoan species. This premetazoan proteome associates with 43% of all annotated human biological processes. Subsequently, four major waves of innovations can be inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi (bony vertebrates), and hominidae, largely specific to each epoch, whereas early branching deuterostome and chordate phyla show very few innovations. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

Show MeSH