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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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Evolution of the respective sizes of the human, Drosophila, Capitella, and Hydra orthologomes. Sequences of the Hydra, Drosophila, Capitella, and human proteomes were used to size independently orthologomes on representative eukaryotes. Timings of radiations were taken from Battacharya et al. (2009) for holozoans; from Peterson et al. (2008) for metazoans, eumetazoans, bilaterians, deuterostomes, and vertebrates; from Steiper and Young (2009) for primates. We arbitrarily placed Chordata origin at midtime between Deuterostomia and Vertebrata origins in agreement with Ayala et al. (1998). Each bar represents the number of RBHs obtained between human (black), Capitella (red), Drosophila (yellow), and Hydra (gray) proteomes and the indicated species. Size of the orthologomes is given for human and Hydra. Note the impact of proteome completeness with the two Saccoglossus data sets.
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evt142-F2: Evolution of the respective sizes of the human, Drosophila, Capitella, and Hydra orthologomes. Sequences of the Hydra, Drosophila, Capitella, and human proteomes were used to size independently orthologomes on representative eukaryotes. Timings of radiations were taken from Battacharya et al. (2009) for holozoans; from Peterson et al. (2008) for metazoans, eumetazoans, bilaterians, deuterostomes, and vertebrates; from Steiper and Young (2009) for primates. We arbitrarily placed Chordata origin at midtime between Deuterostomia and Vertebrata origins in agreement with Ayala et al. (1998). Each bar represents the number of RBHs obtained between human (black), Capitella (red), Drosophila (yellow), and Hydra (gray) proteomes and the indicated species. Size of the orthologomes is given for human and Hydra. Note the impact of proteome completeness with the two Saccoglossus data sets.

Mentions: To measure the variations in orthologome sizes between different phyla, we first tested the human, Drosophila, Capitella, and Hydra proteomes on noneumetazoan species and recorded similar orthologome sizes, 3,000–3,200 large with Arabidopsis and Dictyostelium, 2,000 with S. cerevisiae, 3,500–4,000 with Capsaspora and the choanoflagellates Monosiga and Salpingoeca, up to 5,200–5,500 with Amphimedon (fig. 2). The Saccharomyces orthologomes do not reflect the protein equipment of the fungi LCA, because the S. cerevisiae genome underwent a drastic reduction when compared with other fungi (Cliften et al. 2006). Indeed, we detected larger orthologomes for four other fungi, ranging from 2,410 to 3,315 (supplementary fig. S3A, Supplementary Material online). Similarly, Drosophila orthologomes are consistently smaller (yellow bars), indicating that this species also underwent significant gene losses. Indeed, none of the Drosophila-cnidarian orthologomes reach 5,000, whereas the human, Capitella, and Hydra orthologomes tested on cnidarian proteomes exhibit significantly larger sizes (6,696, 7,191, and 7,138, respectively, with Nematostella).Fig. 2.—


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

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

Evolution of the respective sizes of the human, Drosophila, Capitella, and Hydra orthologomes. Sequences of the Hydra, Drosophila, Capitella, and human proteomes were used to size independently orthologomes on representative eukaryotes. Timings of radiations were taken from Battacharya et al. (2009) for holozoans; from Peterson et al. (2008) for metazoans, eumetazoans, bilaterians, deuterostomes, and vertebrates; from Steiper and Young (2009) for primates. We arbitrarily placed Chordata origin at midtime between Deuterostomia and Vertebrata origins in agreement with Ayala et al. (1998). Each bar represents the number of RBHs obtained between human (black), Capitella (red), Drosophila (yellow), and Hydra (gray) proteomes and the indicated species. Size of the orthologomes is given for human and Hydra. Note the impact of proteome completeness with the two Saccoglossus data sets.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt142-F2: Evolution of the respective sizes of the human, Drosophila, Capitella, and Hydra orthologomes. Sequences of the Hydra, Drosophila, Capitella, and human proteomes were used to size independently orthologomes on representative eukaryotes. Timings of radiations were taken from Battacharya et al. (2009) for holozoans; from Peterson et al. (2008) for metazoans, eumetazoans, bilaterians, deuterostomes, and vertebrates; from Steiper and Young (2009) for primates. We arbitrarily placed Chordata origin at midtime between Deuterostomia and Vertebrata origins in agreement with Ayala et al. (1998). Each bar represents the number of RBHs obtained between human (black), Capitella (red), Drosophila (yellow), and Hydra (gray) proteomes and the indicated species. Size of the orthologomes is given for human and Hydra. Note the impact of proteome completeness with the two Saccoglossus data sets.
Mentions: To measure the variations in orthologome sizes between different phyla, we first tested the human, Drosophila, Capitella, and Hydra proteomes on noneumetazoan species and recorded similar orthologome sizes, 3,000–3,200 large with Arabidopsis and Dictyostelium, 2,000 with S. cerevisiae, 3,500–4,000 with Capsaspora and the choanoflagellates Monosiga and Salpingoeca, up to 5,200–5,500 with Amphimedon (fig. 2). The Saccharomyces orthologomes do not reflect the protein equipment of the fungi LCA, because the S. cerevisiae genome underwent a drastic reduction when compared with other fungi (Cliften et al. 2006). Indeed, we detected larger orthologomes for four other fungi, ranging from 2,410 to 3,315 (supplementary fig. S3A, Supplementary Material online). Similarly, Drosophila orthologomes are consistently smaller (yellow bars), indicating that this species also underwent significant gene losses. Indeed, none of the Drosophila-cnidarian orthologomes reach 5,000, whereas the human, Capitella, and Hydra orthologomes tested on cnidarian proteomes exhibit significantly larger sizes (6,696, 7,191, and 7,138, respectively, with Nematostella).Fig. 2.—

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