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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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Expansion of human orthologs in the LCAs of metazoans, eumetazoans, and bilaterians. (A) Plot showing the RBH scores obtained by 20,231 human proteins tested on seven noneumetazoan proteomes (x axis, Groups I and II) and on four cnidarian proteomes (y axis, Group III). Among these, 7,789 were present in the LCAs of metazoans (I, II), 2,422 (12%) originated in the LCAs of eumetazoans (Group III), and 10,020 (49.5%) represent postcnidarian novelties (Group IV). Note the distribution of proteins involved in human mesoderm development (blue) and ribosome biogenesis (red). (B) Scheme recapitulating the prebilaterian evolutionary events of human proteins: Emergences (star), losses (empty square), and family expansions (triangle). For species abbreviations, see figure 2.
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evt142-F3: Expansion of human orthologs in the LCAs of metazoans, eumetazoans, and bilaterians. (A) Plot showing the RBH scores obtained by 20,231 human proteins tested on seven noneumetazoan proteomes (x axis, Groups I and II) and on four cnidarian proteomes (y axis, Group III). Among these, 7,789 were present in the LCAs of metazoans (I, II), 2,422 (12%) originated in the LCAs of eumetazoans (Group III), and 10,020 (49.5%) represent postcnidarian novelties (Group IV). Note the distribution of proteins involved in human mesoderm development (blue) and ribosome biogenesis (red). (B) Scheme recapitulating the prebilaterian evolutionary events of human proteins: Emergences (star), losses (empty square), and family expansions (triangle). For species abbreviations, see figure 2.

Mentions: To analyze the origins of the human protein complement, we first extracted the core metazoan orthologome, which comprises orthologs shared between humans and at least one cnidarian and one noneumetazoan species (fig. 3, Group I). This core metazoan orthologome contains 6,701 proteins that account for 33.1% of the 20,231 human proteins used in this study; 4,043 proteins (60%) are affiliated to huBPs containing the word “metabolic” and are thus presumably involved in metabolic functions (ribosome biogenesis, transcription, translation, cell cycle regulation). We then inferred two complementary groups that originated prior to bilaterians. Group II contains 1,087 human orthologs (5.4%) detected in noneumetazoan species but no longer found in cnidarians, thus originating before eumetazoans but lost or highly divergent in cnidarians. Group III contains 2,422 human proteins (12%) that emerged with eumetazoan LCAs as evidenced by their presence in at least one cnidarian species but their absence in noneumetazoan species (figs. 3A and 3B). Thus, Group III represents potential eumetazoan novelties. Finally, 10,021 human proteins (49.5%, Group IV) could not be affiliated to orthologs in nonbilaterian proteomes, indicating that they most likely emerged after Cnidaria divergence. Hence, by analyzing the orthologous relationships of each human protein, we could deduce the period when most of them emerged, premetazoan for 38.5%, protoeumetazoan for 12%, and protobilaterian or bilaterian for 49.5%.Fig. 3.—


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

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

Expansion of human orthologs in the LCAs of metazoans, eumetazoans, and bilaterians. (A) Plot showing the RBH scores obtained by 20,231 human proteins tested on seven noneumetazoan proteomes (x axis, Groups I and II) and on four cnidarian proteomes (y axis, Group III). Among these, 7,789 were present in the LCAs of metazoans (I, II), 2,422 (12%) originated in the LCAs of eumetazoans (Group III), and 10,020 (49.5%) represent postcnidarian novelties (Group IV). Note the distribution of proteins involved in human mesoderm development (blue) and ribosome biogenesis (red). (B) Scheme recapitulating the prebilaterian evolutionary events of human proteins: Emergences (star), losses (empty square), and family expansions (triangle). For species abbreviations, see figure 2.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt142-F3: Expansion of human orthologs in the LCAs of metazoans, eumetazoans, and bilaterians. (A) Plot showing the RBH scores obtained by 20,231 human proteins tested on seven noneumetazoan proteomes (x axis, Groups I and II) and on four cnidarian proteomes (y axis, Group III). Among these, 7,789 were present in the LCAs of metazoans (I, II), 2,422 (12%) originated in the LCAs of eumetazoans (Group III), and 10,020 (49.5%) represent postcnidarian novelties (Group IV). Note the distribution of proteins involved in human mesoderm development (blue) and ribosome biogenesis (red). (B) Scheme recapitulating the prebilaterian evolutionary events of human proteins: Emergences (star), losses (empty square), and family expansions (triangle). For species abbreviations, see figure 2.
Mentions: To analyze the origins of the human protein complement, we first extracted the core metazoan orthologome, which comprises orthologs shared between humans and at least one cnidarian and one noneumetazoan species (fig. 3, Group I). This core metazoan orthologome contains 6,701 proteins that account for 33.1% of the 20,231 human proteins used in this study; 4,043 proteins (60%) are affiliated to huBPs containing the word “metabolic” and are thus presumably involved in metabolic functions (ribosome biogenesis, transcription, translation, cell cycle regulation). We then inferred two complementary groups that originated prior to bilaterians. Group II contains 1,087 human orthologs (5.4%) detected in noneumetazoan species but no longer found in cnidarians, thus originating before eumetazoans but lost or highly divergent in cnidarians. Group III contains 2,422 human proteins (12%) that emerged with eumetazoan LCAs as evidenced by their presence in at least one cnidarian species but their absence in noneumetazoan species (figs. 3A and 3B). Thus, Group III represents potential eumetazoan novelties. Finally, 10,021 human proteins (49.5%, Group IV) could not be affiliated to orthologs in nonbilaterian proteomes, indicating that they most likely emerged after Cnidaria divergence. Hence, by analyzing the orthologous relationships of each human protein, we could deduce the period when most of them emerged, premetazoan for 38.5%, protoeumetazoan for 12%, and protobilaterian or bilaterian for 49.5%.Fig. 3.—

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
Related in: MedlinePlus