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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 ortholog-deduced Biological Processes (huBPs) emerged in the LCAs of metazoans (A), bilaterians (B), chordates (C), vertebrates (D), and primates (E). BPs showing protein enrichment ≥2 times (horizontal scale) are depicted by a circle whose surface is proportional to the number of proteins. The color code indicates two levels of statistical significance (see inset). Note the significantly enriched huBPs in LCAs of each period (see table 2): Embryonic development in protometazoans; neurogenesis, organ morphogenesis and regulation of transcription in protoeumetazoans; nervous system development and regulation of biosynthetic process in protobilaterians; muscle tissue development in protochordates; cell adhesion, response to external stimulus, G-protein coupled receptor signaling pathway and inflammatory response in vertebrates; sensory perception and defense response to bacterium in primates; complement activation, humoral immune response, and leukocyte-mediated immunity in hominidae. For the full list of protein-enriched BPs, see supplementary table S2, Supplementary Material online.
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evt142-F5: Characterization of the ortholog-deduced Biological Processes (huBPs) emerged in the LCAs of metazoans (A), bilaterians (B), chordates (C), vertebrates (D), and primates (E). BPs showing protein enrichment ≥2 times (horizontal scale) are depicted by a circle whose surface is proportional to the number of proteins. The color code indicates two levels of statistical significance (see inset). Note the significantly enriched huBPs in LCAs of each period (see table 2): Embryonic development in protometazoans; neurogenesis, organ morphogenesis and regulation of transcription in protoeumetazoans; nervous system development and regulation of biosynthetic process in protobilaterians; muscle tissue development in protochordates; cell adhesion, response to external stimulus, G-protein coupled receptor signaling pathway and inflammatory response in vertebrates; sensory perception and defense response to bacterium in primates; complement activation, humoral immune response, and leukocyte-mediated immunity in hominidae. For the full list of protein-enriched BPs, see supplementary table S2, Supplementary Material online.

Mentions: The 6,670 human orthologs detected in at least one nonmetazoan species distribute into 530 protein-enriched BPs (fig. 4A), which, similarly to the core metazoan orthologome (Group I, fig. 3A), associate with huBPs predominantly related to metabolic processes (75%, table 2, supplementary table S2, Supplementary Material online). By contrast the 1,119 novel orthologs identified in Amphimedon proteome associates with 60 protein-enriched BPs (fig. 4A) mostly related to embryonic development (fig. 5A, table 2 and supplementary table S2, Supplementary Material online). This rather low number of novel proteins and associated BP in porifers is in agreement with the notion that transitions from unicellularity to multicellularity might have required a limited number of genetic innovations (Grosberg and Strathmann 2007; Ratcliff et al. 2012). However, the data set from porifers is still limited; therefore, some of the protein gains currently mapped to the eumetazoan transition might receive an earlier origin when genomic information will be extended to more porifer species.Fig. 5.—


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 ortholog-deduced Biological Processes (huBPs) emerged in the LCAs of metazoans (A), bilaterians (B), chordates (C), vertebrates (D), and primates (E). BPs showing protein enrichment ≥2 times (horizontal scale) are depicted by a circle whose surface is proportional to the number of proteins. The color code indicates two levels of statistical significance (see inset). Note the significantly enriched huBPs in LCAs of each period (see table 2): Embryonic development in protometazoans; neurogenesis, organ morphogenesis and regulation of transcription in protoeumetazoans; nervous system development and regulation of biosynthetic process in protobilaterians; muscle tissue development in protochordates; cell adhesion, response to external stimulus, G-protein coupled receptor signaling pathway and inflammatory response in vertebrates; sensory perception and defense response to bacterium in primates; complement activation, humoral immune response, and leukocyte-mediated immunity in hominidae. For the full list of protein-enriched BPs, see supplementary table S2, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt142-F5: Characterization of the ortholog-deduced Biological Processes (huBPs) emerged in the LCAs of metazoans (A), bilaterians (B), chordates (C), vertebrates (D), and primates (E). BPs showing protein enrichment ≥2 times (horizontal scale) are depicted by a circle whose surface is proportional to the number of proteins. The color code indicates two levels of statistical significance (see inset). Note the significantly enriched huBPs in LCAs of each period (see table 2): Embryonic development in protometazoans; neurogenesis, organ morphogenesis and regulation of transcription in protoeumetazoans; nervous system development and regulation of biosynthetic process in protobilaterians; muscle tissue development in protochordates; cell adhesion, response to external stimulus, G-protein coupled receptor signaling pathway and inflammatory response in vertebrates; sensory perception and defense response to bacterium in primates; complement activation, humoral immune response, and leukocyte-mediated immunity in hominidae. For the full list of protein-enriched BPs, see supplementary table S2, Supplementary Material online.
Mentions: The 6,670 human orthologs detected in at least one nonmetazoan species distribute into 530 protein-enriched BPs (fig. 4A), which, similarly to the core metazoan orthologome (Group I, fig. 3A), associate with huBPs predominantly related to metabolic processes (75%, table 2, supplementary table S2, Supplementary Material online). By contrast the 1,119 novel orthologs identified in Amphimedon proteome associates with 60 protein-enriched BPs (fig. 4A) mostly related to embryonic development (fig. 5A, table 2 and supplementary table S2, Supplementary Material online). This rather low number of novel proteins and associated BP in porifers is in agreement with the notion that transitions from unicellularity to multicellularity might have required a limited number of genetic innovations (Grosberg and Strathmann 2007; Ratcliff et al. 2012). However, the data set from porifers is still limited; therefore, some of the protein gains currently mapped to the eumetazoan transition might receive an earlier origin when genomic information will be extended to more porifer species.Fig. 5.—

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