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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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RBH computing. The RBH process takes place after a reasonably complete proteome (here human) is aligned unidirectionally to another whole proteome (here Hydra). (A) After BlastP+ (e value 10−10) relations between the human and Hydra protein sets are established, represented by a series of basal hits between either a given human protein and several Hydra proteins (black arrows) or inferred between a given Hydra protein and several human proteins (gray arrows). Each of these relationships receives a Blast score (numbers next to the arrows) that is valid for both the query–hit and the hit–query relationships. (B) Relations that are retained as RBHs fulfill two criteria: 1) Best score between a given query and the different hits (red arrow) and 2) best score between a given hit and the different queries (blue arrow). (C) In the case where two or more query/hit relationships with a shared query or hit qualify as RBH, one pair is selected randomly. This scenario typically takes places when nearly identical paralog sequences are present in the query or target proteomes.
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evt142-F1: RBH computing. The RBH process takes place after a reasonably complete proteome (here human) is aligned unidirectionally to another whole proteome (here Hydra). (A) After BlastP+ (e value 10−10) relations between the human and Hydra protein sets are established, represented by a series of basal hits between either a given human protein and several Hydra proteins (black arrows) or inferred between a given Hydra protein and several human proteins (gray arrows). Each of these relationships receives a Blast score (numbers next to the arrows) that is valid for both the query–hit and the hit–query relationships. (B) Relations that are retained as RBHs fulfill two criteria: 1) Best score between a given query and the different hits (red arrow) and 2) best score between a given hit and the different queries (blue arrow). (C) In the case where two or more query/hit relationships with a shared query or hit qualify as RBH, one pair is selected randomly. This scenario typically takes places when nearly identical paralog sequences are present in the query or target proteomes.

Mentions: The human, Capitella, Drosophila, and Hydra proteomes were used as input for BlastP+ using a maximum e value threshold of 10−10, with soft masking as suggested by (Moreno-Hagelsieb and Latimer 2008). Relations retained as RBHs fulfilled two criteria (fig. 1): 1) best score between a given query and the different hits (red arrow), 2) best score between a given hit and the different queries (blue arrows). Query/hit pairs satisfying only one of the two criteria above were assigned an alignment bit score of 10, whereas queries with no blast hit were assigned an alignment bit score of 1.Fig. 1.—


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

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

RBH computing. The RBH process takes place after a reasonably complete proteome (here human) is aligned unidirectionally to another whole proteome (here Hydra). (A) After BlastP+ (e value 10−10) relations between the human and Hydra protein sets are established, represented by a series of basal hits between either a given human protein and several Hydra proteins (black arrows) or inferred between a given Hydra protein and several human proteins (gray arrows). Each of these relationships receives a Blast score (numbers next to the arrows) that is valid for both the query–hit and the hit–query relationships. (B) Relations that are retained as RBHs fulfill two criteria: 1) Best score between a given query and the different hits (red arrow) and 2) best score between a given hit and the different queries (blue arrow). (C) In the case where two or more query/hit relationships with a shared query or hit qualify as RBH, one pair is selected randomly. This scenario typically takes places when nearly identical paralog sequences are present in the query or target proteomes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt142-F1: RBH computing. The RBH process takes place after a reasonably complete proteome (here human) is aligned unidirectionally to another whole proteome (here Hydra). (A) After BlastP+ (e value 10−10) relations between the human and Hydra protein sets are established, represented by a series of basal hits between either a given human protein and several Hydra proteins (black arrows) or inferred between a given Hydra protein and several human proteins (gray arrows). Each of these relationships receives a Blast score (numbers next to the arrows) that is valid for both the query–hit and the hit–query relationships. (B) Relations that are retained as RBHs fulfill two criteria: 1) Best score between a given query and the different hits (red arrow) and 2) best score between a given hit and the different queries (blue arrow). (C) In the case where two or more query/hit relationships with a shared query or hit qualify as RBH, one pair is selected randomly. This scenario typically takes places when nearly identical paralog sequences are present in the query or target proteomes.
Mentions: The human, Capitella, Drosophila, and Hydra proteomes were used as input for BlastP+ using a maximum e value threshold of 10−10, with soft masking as suggested by (Moreno-Hagelsieb and Latimer 2008). Relations retained as RBHs fulfilled two criteria (fig. 1): 1) best score between a given query and the different hits (red arrow), 2) best score between a given hit and the different queries (blue arrows). Query/hit pairs satisfying only one of the two criteria above were assigned an alignment bit score of 10, whereas queries with no blast hit were assigned an alignment bit score of 1.Fig. 1.—

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