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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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Characterization of the huBPs associated with major protein gains in cnidarians. (A) Enrichments in proteins for a given huBP were identified in cnidarians (2,422 proteins in Group III) over the 10,211 protobilaterian proteins (Groups I + II + III) as background. The huBPs showing protein enrichment ≥2 times with corrected P values ≤10−5 are shown for cnidarians (red), and noneumetazoans (blue, green). The numbers after each huBP indicate the number of proteins in Groups I, II, III, respectively. The huBPs with protein enrichment ≥2.5x are written bold. For details, see supplementary table S3, Supplementary Material online. (B) Similar gains of novel human orthologs associated with selected huBPs in anthozoan (Acropora, Nematostella) and medusozoan (Hydra) cnidarian proteomes. These three cnidarian species exhibiting widely different lifestyles and morphologies. The scale represents the number of proteins identified in the proteome of each cnidarian species for each indicated huBP.
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evt142-F6: Characterization of the huBPs associated with major protein gains in cnidarians. (A) Enrichments in proteins for a given huBP were identified in cnidarians (2,422 proteins in Group III) over the 10,211 protobilaterian proteins (Groups I + II + III) as background. The huBPs showing protein enrichment ≥2 times with corrected P values ≤10−5 are shown for cnidarians (red), and noneumetazoans (blue, green). The numbers after each huBP indicate the number of proteins in Groups I, II, III, respectively. The huBPs with protein enrichment ≥2.5x are written bold. For details, see supplementary table S3, Supplementary Material online. (B) Similar gains of novel human orthologs associated with selected huBPs in anthozoan (Acropora, Nematostella) and medusozoan (Hydra) cnidarian proteomes. These three cnidarian species exhibiting widely different lifestyles and morphologies. The scale represents the number of proteins identified in the proteome of each cnidarian species for each indicated huBP.

Mentions: The 2,422 novel eumetazoan proteins identified in cnidarians (fig. 3) associate with 242 protein-enriched huBPs; this is the largest number observed throughout the metazoan evolutionary steps selected here (figs. 4A and 4B). To test the robustness of these protein-enriched huBPs, we measured the enrichment of cnidarian proteins either over the human background (as in every other condition) or over the nonbilaterian background. The two methods yielded very similar results on strongly significant BPs (supplementary fig. S5, Supplementary Material online). However cell–cell signaling had a lower significance when tested on the human background rather than on the nonbilaterian background. A major difference exists between these two backgrounds, that is, a second wave of vertebrate-specific expansion of protein families involved in signaling, such as cytokines involved in immune response (fig. 5D), which “dilutes” the original enrichment signal. Beside cell–cell signaling, novel BPs in eumetazoan-LCAs include processes linked to epithelium tube morphogenesis, pattern specification, organ morphogenesis, sensory organ development, regulation of ossification, cell-fate commitment, neurogenesis, and eye development (fig. 6A). At the molecular level, the diversification of the Wnt and BMP signaling pathways and the presence of 183 novel transcription factors appear as robust eumetazoan innovations (supplementary table S3, Supplementary Material online), in agreement with previous reports (Kusserow et al. 2005; Saina et al. 2009; Galliot and Quiquand 2011).Fig. 6.—


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

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

Characterization of the huBPs associated with major protein gains in cnidarians. (A) Enrichments in proteins for a given huBP were identified in cnidarians (2,422 proteins in Group III) over the 10,211 protobilaterian proteins (Groups I + II + III) as background. The huBPs showing protein enrichment ≥2 times with corrected P values ≤10−5 are shown for cnidarians (red), and noneumetazoans (blue, green). The numbers after each huBP indicate the number of proteins in Groups I, II, III, respectively. The huBPs with protein enrichment ≥2.5x are written bold. For details, see supplementary table S3, Supplementary Material online. (B) Similar gains of novel human orthologs associated with selected huBPs in anthozoan (Acropora, Nematostella) and medusozoan (Hydra) cnidarian proteomes. These three cnidarian species exhibiting widely different lifestyles and morphologies. The scale represents the number of proteins identified in the proteome of each cnidarian species for each indicated huBP.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt142-F6: Characterization of the huBPs associated with major protein gains in cnidarians. (A) Enrichments in proteins for a given huBP were identified in cnidarians (2,422 proteins in Group III) over the 10,211 protobilaterian proteins (Groups I + II + III) as background. The huBPs showing protein enrichment ≥2 times with corrected P values ≤10−5 are shown for cnidarians (red), and noneumetazoans (blue, green). The numbers after each huBP indicate the number of proteins in Groups I, II, III, respectively. The huBPs with protein enrichment ≥2.5x are written bold. For details, see supplementary table S3, Supplementary Material online. (B) Similar gains of novel human orthologs associated with selected huBPs in anthozoan (Acropora, Nematostella) and medusozoan (Hydra) cnidarian proteomes. These three cnidarian species exhibiting widely different lifestyles and morphologies. The scale represents the number of proteins identified in the proteome of each cnidarian species for each indicated huBP.
Mentions: The 2,422 novel eumetazoan proteins identified in cnidarians (fig. 3) associate with 242 protein-enriched huBPs; this is the largest number observed throughout the metazoan evolutionary steps selected here (figs. 4A and 4B). To test the robustness of these protein-enriched huBPs, we measured the enrichment of cnidarian proteins either over the human background (as in every other condition) or over the nonbilaterian background. The two methods yielded very similar results on strongly significant BPs (supplementary fig. S5, Supplementary Material online). However cell–cell signaling had a lower significance when tested on the human background rather than on the nonbilaterian background. A major difference exists between these two backgrounds, that is, a second wave of vertebrate-specific expansion of protein families involved in signaling, such as cytokines involved in immune response (fig. 5D), which “dilutes” the original enrichment signal. Beside cell–cell signaling, novel BPs in eumetazoan-LCAs include processes linked to epithelium tube morphogenesis, pattern specification, organ morphogenesis, sensory organ development, regulation of ossification, cell-fate commitment, neurogenesis, and eye development (fig. 6A). At the molecular level, the diversification of the Wnt and BMP signaling pathways and the presence of 183 novel transcription factors appear as robust eumetazoan innovations (supplementary table S3, Supplementary Material online), in agreement with previous reports (Kusserow et al. 2005; Saina et al. 2009; Galliot and Quiquand 2011).Fig. 6.—

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