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Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics.

Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M - BMC Evol. Biol. (2007)

Bottom Line: Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom.We identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica.We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Evolution et Développement des protostomiens, Centre de Génétique Moléculaire- UPR 2167 CNRS, Gif-sur-Yvette Cedex, France. Elena.Simionato@cgm.cnrs-gif.fr <Elena.Simionato@cgm.cnrs-gif.fr>

ABSTRACT

Background: Molecular and genetic analyses conducted in model organisms such as Drosophila and vertebrates, have provided a wealth of information about how networks of transcription factors control the proper development of these species. Much less is known, however, about the evolutionary origin of these elaborated networks and their large-scale evolution. Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom.

Results: We identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica. We have performed extensive phylogenetic analyses of the 695 identified bHLHs, which has allowed us to allocate most of these bHLHs to defined evolutionary conserved groups of orthology.

Conclusion: Three main features in the history of the bHLH gene superfamily can be inferred from these analyses: (i) an initial diversification of the bHLHs has occurred in the pre-Cambrian, prior to metazoan cladogenesis; (ii) a second expansion of the bHLH superfamily occurred early in metazoan evolution before bilaterians and cnidarians diverged; and (iii) the bHLH complement during the evolution of the bilaterians has been remarkably stable. We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.

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Phylogenetic relationships between the species used in this study. The tree is based on the current view of the phylogeny of the metazoans [73,74]. The total number of bHLHs and the number of represented bHLH metazoan families of orthologs in each genome is indicated. For the number of represented families, a range is indicated for most species, due to the uncertainty about the presence of some families in these species (see additional file 1 for details). The names of representative phylogenetic groups are indicated on the left of the nodes that define these different groups and along some of the terminal branches. The Ciona intestinalis data come from [12] and have not been reanalysed in this study.
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Figure 1: Phylogenetic relationships between the species used in this study. The tree is based on the current view of the phylogeny of the metazoans [73,74]. The total number of bHLHs and the number of represented bHLH metazoan families of orthologs in each genome is indicated. For the number of represented families, a range is indicated for most species, due to the uncertainty about the presence of some families in these species (see additional file 1 for details). The names of representative phylogenetic groups are indicated on the left of the nodes that define these different groups and along some of the terminal branches. The Ciona intestinalis data come from [12] and have not been reanalysed in this study.

Mentions: Based on the analysis of the putative full-set of bHLH genes from Drosophila melanogaster, Caenorhabditis elegans, and Homo sapiens, we previously defined 44 orthologous families that include most of these bHLHs [4,11]. Of these, 43 include genes from Homo sapiens, and Drosophila melanogaster and/or Caenorhabditis elegans, indicating that these families were already present in the last common ancestor of these three species, thus of all bilaterians. This study led us to conclude that the diversification of the bHLH complement independently occurred in metazoans and plants and might have been related to the acquisition of multicellularity [11]. In the present study, we identified the putative full set of bHLHs encoded by several newly sequenced genomes of species representative of the main metazoan evolutionary lineages (Figure 1). Of special interest, we obtained data from three non-bilaterian species, two cnidarians and a demosponge, providing us with the opportunity to study the early evolutionary history of the bHLH superfamily in metazoans. Phylogenetic analysis of the sequence of these bHLHs allows us to conclude that (i) most of the bHLH bilaterian families of orthologs are present in cnidarians; (ii) only a few families are present in a demosponge species; (iii) the number of represented bHLH families of orthologs is remarkably similar in the different bilaterian lineages. We propose an evolutionary scenario in which the diversity of metazoan bHLHs has been established in two main steps, one during the early evolution of metazoans, before the divergence of demosponges from other metazoans, and the second, later, after this split but before the divergence of cnidarians and bilaterians.


Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics.

Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M - BMC Evol. Biol. (2007)

Phylogenetic relationships between the species used in this study. The tree is based on the current view of the phylogeny of the metazoans [73,74]. The total number of bHLHs and the number of represented bHLH metazoan families of orthologs in each genome is indicated. For the number of represented families, a range is indicated for most species, due to the uncertainty about the presence of some families in these species (see additional file 1 for details). The names of representative phylogenetic groups are indicated on the left of the nodes that define these different groups and along some of the terminal branches. The Ciona intestinalis data come from [12] and have not been reanalysed in this study.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1828162&req=5

Figure 1: Phylogenetic relationships between the species used in this study. The tree is based on the current view of the phylogeny of the metazoans [73,74]. The total number of bHLHs and the number of represented bHLH metazoan families of orthologs in each genome is indicated. For the number of represented families, a range is indicated for most species, due to the uncertainty about the presence of some families in these species (see additional file 1 for details). The names of representative phylogenetic groups are indicated on the left of the nodes that define these different groups and along some of the terminal branches. The Ciona intestinalis data come from [12] and have not been reanalysed in this study.
Mentions: Based on the analysis of the putative full-set of bHLH genes from Drosophila melanogaster, Caenorhabditis elegans, and Homo sapiens, we previously defined 44 orthologous families that include most of these bHLHs [4,11]. Of these, 43 include genes from Homo sapiens, and Drosophila melanogaster and/or Caenorhabditis elegans, indicating that these families were already present in the last common ancestor of these three species, thus of all bilaterians. This study led us to conclude that the diversification of the bHLH complement independently occurred in metazoans and plants and might have been related to the acquisition of multicellularity [11]. In the present study, we identified the putative full set of bHLHs encoded by several newly sequenced genomes of species representative of the main metazoan evolutionary lineages (Figure 1). Of special interest, we obtained data from three non-bilaterian species, two cnidarians and a demosponge, providing us with the opportunity to study the early evolutionary history of the bHLH superfamily in metazoans. Phylogenetic analysis of the sequence of these bHLHs allows us to conclude that (i) most of the bHLH bilaterian families of orthologs are present in cnidarians; (ii) only a few families are present in a demosponge species; (iii) the number of represented bHLH families of orthologs is remarkably similar in the different bilaterian lineages. We propose an evolutionary scenario in which the diversity of metazoan bHLHs has been established in two main steps, one during the early evolution of metazoans, before the divergence of demosponges from other metazoans, and the second, later, after this split but before the divergence of cnidarians and bilaterians.

Bottom Line: Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom.We identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica.We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Evolution et Développement des protostomiens, Centre de Génétique Moléculaire- UPR 2167 CNRS, Gif-sur-Yvette Cedex, France. Elena.Simionato@cgm.cnrs-gif.fr <Elena.Simionato@cgm.cnrs-gif.fr>

ABSTRACT

Background: Molecular and genetic analyses conducted in model organisms such as Drosophila and vertebrates, have provided a wealth of information about how networks of transcription factors control the proper development of these species. Much less is known, however, about the evolutionary origin of these elaborated networks and their large-scale evolution. Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom.

Results: We identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica. We have performed extensive phylogenetic analyses of the 695 identified bHLHs, which has allowed us to allocate most of these bHLHs to defined evolutionary conserved groups of orthology.

Conclusion: Three main features in the history of the bHLH gene superfamily can be inferred from these analyses: (i) an initial diversification of the bHLHs has occurred in the pre-Cambrian, prior to metazoan cladogenesis; (ii) a second expansion of the bHLH superfamily occurred early in metazoan evolution before bilaterians and cnidarians diverged; and (iii) the bHLH complement during the evolution of the bilaterians has been remarkably stable. We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.

Show MeSH