Publications by authors named "Michel Vervoort"

39 Publications

[A trio of mechanisms involved in regeneration initiation in animals].

Med Sci (Paris) 2021 Apr 28;37(4):349-358. Epub 2021 Apr 28.

Université de Paris, CNRS, Institut Jacques Monod, F-75006 Paris, France.

Whole-body and complex structure regeneration is a widespread phenomenon in animals. While regenerative abilities vary greatly from one species to another, a number of mechanisms appear essential for regeneration in distantly related phylogenetic groups. In this review, we synthetize the knowledge gathered on the implication of three mechanisms that appear to be important for the initiation of regeneration in animals. Reactive Oxygen Species (ROS) are metabolic by-products involved in cell signalling, which are produced shortly after amputation in several species. ROS production may be responsible for triggering apoptosis, another recurring mechanism involved in regeneration initiation. In turn, apoptosis causes compensatory proliferation by setting off cellular division, thus contributing to the reconstitution of tissues. Inhibiting either ROS production, apoptosis or cellular proliferation impairs regeneration in a variety of model species.
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http://dx.doi.org/10.1051/medsci/2021037DOI Listing
April 2021

Animal regeneration in the era of transcriptomics.

Cell Mol Life Sci 2021 Apr 30;78(8):3941-3956. Epub 2021 Jan 30.

Université de Paris, CNRS, Institut Jacques Monod, 75006, Paris, France.

Animal regeneration, the ability to restore a lost body part, is a process that has fascinated scientists for centuries. In this review, we first present what regeneration is and how it relates to development, as well as the widespread and diverse nature of regeneration in animals. Despite this diversity, animal regeneration includes three common mechanistic steps: initiation, induction and activation of progenitors, and morphogenesis. In this review article, we summarize and discuss, from an evolutionary perspective, the recent data obtained for a variety of regeneration models which have allowed to identify key shared mechanisms that control these main steps of animal regeneration. This review also synthesizes the wealth of high-throughput mRNA sequencing data (bulk mRNA-seq) concerning regeneration which have been obtained in recent years, highlighting the major advances in the regeneration field that these studies have revealed. We stress out that, through a comparative approach, these data provide opportunities to further shed light on the evolution of regeneration in animals. Finally, we point out how the use of single-cell mRNA-seq technology and integration with epigenomic approaches may further help researchers to decipher mechanisms controlling regeneration and their evolution in animals.
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http://dx.doi.org/10.1007/s00018-021-03760-7DOI Listing
April 2021

Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii.

Dev Biol 2019 01 13;445(2):189-210. Epub 2018 Nov 13.

Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, F-75205 Paris, France. Electronic address:

Regeneration, the ability to restore body parts after an injury or an amputation, is a widespread but highly variable and complex phenomenon in animals. While having fascinated scientists for centuries, fundamental questions about the cellular basis of animal regeneration as well as its evolutionary history remain largely unanswered. Here, we present a study of regeneration of the marine annelid Platynereis dumerilii, an emerging comparative developmental biology model, which, like many other annelids, displays important regenerative abilities. When P. dumerilii worms are amputated, they are able to regenerate the posteriormost differentiated part of their body and a stem cell-rich growth zone that allows the production of new segments replacing the amputated ones. We show that posterior regeneration is a rapid process that follows a well reproducible path and timeline, going through specific stages that we thoroughly defined. Wound healing is achieved one day after amputation and a regeneration blastema forms one day later. At this time point, some tissue specification already occurs, and a functional posterior growth zone is re-established as early as three days after amputation. Regeneration timing is only influenced, in a minor manner, by worm size. Comparable regenerative abilities are found for amputations performed at different positions along the antero-posterior axis of the worm, except when amputation planes are very close to the pharynx. Regenerative abilities persist upon repeated amputations without important alterations of the process. We also show that intense cell proliferation occurs during regeneration and that cell divisions are required for regeneration to proceed normally. Finally, 5-ethynyl-2'-deoxyuridine (EdU) pulse and chase experiments suggest that blastemal cells mostly derive from the segment immediately abutting the amputation plane. The detailed characterization of P. dumerilii posterior body regeneration presented in this article provides the foundation for future mechanistic and comparative studies of regeneration in this species.
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http://dx.doi.org/10.1016/j.ydbio.2018.11.004DOI Listing
January 2019

Cell lineage and cell cycling analyses of the 4d micromere using live imaging in the marine annelid .

Elife 2017 12 12;6. Epub 2017 Dec 12.

Institut Jacques Monod, Paris, France.

Cell lineage, cell cycle, and cell fate are tightly associated in developmental processes, but in vivo studies at single-cell resolution showing the intricacies of these associations are rare due to technical limitations. In this study on the marine annelid we investigated the lineage of the 4d micromere, using high-resolution long-term live imaging complemented with a live-cell cycle reporter. 4d is the origin of mesodermal lineages and the germline in many spiralians. We traced lineages at single-cell resolution within 4d and demonstrate that embryonic segmental mesoderm forms via teloblastic divisions, as in clitellate annelids. We also identified the precise cellular origins of the larval mesodermal posterior growth zone. We found that differentially-fated progeny of 4d (germline, segmental mesoderm, growth zone) display significantly different cell cycling. This work has evolutionary implications, sets up the foundation for functional studies in annelid stem cells, and presents newly established techniques for live imaging marine embryos.
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http://dx.doi.org/10.7554/eLife.30463DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5764573PMC
December 2017

Conservation and divergence of bHLH genes in the calcisponge .

Evodevo 2016 14;7:23. Epub 2016 Oct 14.

Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.

Background: Basic Helix-Loop-Helix (bHLH) genes encode a large family of eukaryotic transcription factors, categorized into six high-order groups: pan-eukaryotic group B involved in regulation of cell cycle, metabolism, and development; holozoan-specific groups C and F involved in development and maintenance of homeostasis; and metazoan-specific groups A, D and E including well-studied genes, such as , and , with diverse developmental roles including control of morphogenesis and specification of neurons. Current scenarios of bHLH evolution in animals are mainly based on the bHLH gene set found in the genome of demosponge In this species, the majority of the 21 identified bHLH genes belong to group B, and the single group A gene is orthologous to several neurogenic bilaterian subfamilies, including and .

Results: Given recently discovered differences in developmental toolkit components between siliceous and calcareous sponges, we have carried out genome-wide analysis of bHLH genes in , an emerging calcisponge model. We identified 30 bHLH genes in this species, representing 12 individual families, including four group A families not found in , and two larger family groupings. Notably, the families represented in are only partially overlapping with those represented in Developmental expression analysis of a subset of the identified genes revealed patterns consistent with deeply conserved roles, such as specification of sensory cells by - and stem cells by genes.

Conclusions: Our results demonstrate independent gene loss events in demosponges and calcisponges, implying a complex bHLH toolkit in the last common metazoan ancestor.
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http://dx.doi.org/10.1186/s13227-016-0060-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5064789PMC
October 2016

Neuronal fate specification by the Dbx1 transcription factor is linked to the evolutionary acquisition of a novel functional domain.

Evodevo 2016 12;7:18. Epub 2016 Aug 12.

Dept. BEOM, Stazione Zoologica A. Dohrn, Villa Comunale, 80121 Naples, Italy.

Background: Dbx1 is a homeodomain transcription factor involved in neuronal fate specification belonging to a widely conserved family among bilaterians. In mammals, Dbx1 was proposed to act as a transcriptional repressor by interacting with the Groucho corepressors to allow the specification of neurons involved in essential biological functions such as locomotion or breathing.

Results: Sequence alignments of Dbx1 proteins from different species allowed us to identify two conserved domains related to the Groucho-dependent Engrailed repressor domain (RD), as well as a newly described domain composed of clusterized acidic residues at the C-terminus (Cter) which is present in tetrapods but also several invertebrates. Using a heterologous luciferase assay, we showed that the two putative repressor domains behave as such in a Groucho-dependent manner, whereas the Cter does not bear any intrinsic transcriptional activity. Consistently with in vitro data, we found that both RDs are involved in cell fate specification using in vivo electroporation experiments in the chick spinal cord. Surprisingly, we show that the Cter domain is required for Dbx1 function in vivo, acting as a modulator of its repressive activity and/or imparting specificity.

Conclusion: Our results strongly suggest that the presence of a Cter domain among tetrapods is essential for Dbx1 to regulate neuronal diversity and, in turn, nervous system complexity.
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http://dx.doi.org/10.1186/s13227-016-0055-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4983035PMC
August 2016

Defining "Development".

Curr Top Dev Biol 2016 1;117:171-83. Epub 2016 Feb 1.

Institut Jacques Monod, CNRS, UMR 7592, Univ Paris Diderot, Sorbonne Paris Cité, Paris, France.

Is it possible, and in the first place is it even desirable, to define what "development" means and to determine the scope of the field called "developmental biology"? Though these questions appeared crucial for the founders of "developmental biology" in the 1950s, there seems to be no consensus today about the need to address them. Here, in a combined biological, philosophical, and historical approach, we ask whether it is possible and useful to define biological development, and, if such a definition is indeed possible and useful, which definition(s) can be considered as the most satisfactory.
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http://dx.doi.org/10.1016/bs.ctdb.2015.10.012DOI Listing
December 2016

Evolution of Prdm Genes in Animals: Insights from Comparative Genomics.

Mol Biol Evol 2016 Mar 11;33(3):679-96. Epub 2015 Nov 11.

Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France

Prdm genes encode transcription factors with a subtype of SET domain known as the PRDF1-RIZ (PR) homology domain and a variable number of zinc finger motifs. These genes are involved in a wide variety of functions during animal development. As most Prdm genes have been studied in vertebrates, especially in mice, little is known about the evolution of this gene family. We searched for Prdm genes in the fully sequenced genomes of 93 different species representative of all the main metazoan lineages. A total of 976 Prdm genes were identified in these species. The number of Prdm genes per species ranges from 2 to 19. To better understand how the Prdm gene family has evolved in metazoans, we performed phylogenetic analyses using this large set of identified Prdm genes. These analyses allowed us to define 14 different subfamilies of Prdm genes and to establish, through ancestral state reconstruction, that 11 of them are ancestral to bilaterian animals. Three additional subfamilies were acquired during early vertebrate evolution (Prdm5, Prdm11, and Prdm17). Several gene duplication and gene loss events were identified and mapped onto the metazoan phylogenetic tree. By studying a large number of nonmetazoan genomes, we confirmed that Prdm genes likely constitute a metazoan-specific gene family. Our data also suggest that Prdm genes originated before the diversification of animals through the association of a single ancestral SET domain encoding gene with one or several zinc finger encoding genes.
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http://dx.doi.org/10.1093/molbev/msv260DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760075PMC
March 2016

A metameric origin for the annelid pygidium?

BMC Evol Biol 2015 Feb 25;15:25. Epub 2015 Feb 25.

Institut Jacques Monod, CNRS/Université Paris Diderot, 15 rue Hélène Brion, 75013, Paris, France.

Background: Segmented body organizations are widely represented in the animal kingdom. Whether the last common bilaterian ancestor was already segmented is intensely debated. Annelids display broad morphological diversity but many species are among the most homonomous metameric animals. The front end (prostomium) and tail piece (pygidium) of annelids are classically described as non-segmental. However, the pygidium structure and development remain poorly studied.

Results: Using different methods of microscopy, immunolabelling and a number of molecular markers, we describe the neural and mesodermal structures of the pygidium of Platynereis dumerilii. We establish that the pygidium possesses a complicated nervous system with a nerve ring and a pair of sensory ganglia, a complex intrinsic musculature, a large terminal circular blood sinus and an unusual unpaired torus-shaped coelomic cavity. We also describe some earlier steps of pygidial development and pygidial structure of mature animals after epitokous transformation.

Conclusions: We describe a much more complex organization of the pygidium of P. dumerilii than previously suggested. Many of the characteristics are strikingly similar to those found in the trunk segments, opening the debate on whether the pygidium and trunk segments derive from the same ancestral metameric unit. We analyze these scenarios in the context of two classical theories on the origin of segmentation: the cyclomeric/archicoelomate concept and the colonial theory. Both theories provide possible explanations for the partial or complete homology of trunk segments and pygidium.
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http://dx.doi.org/10.1186/s12862-015-0299-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4357181PMC
February 2015

Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements.

PLoS Genet 2014 Sep 25;10(9):e1004665. Epub 2014 Sep 25.

Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France.

In the ciliate Paramecium tetraurelia, differentiation of the somatic nucleus from the zygotic nucleus is characterized by massive and reproducible deletion of transposable elements and of 45,000 short, dispersed, single-copy sequences. A specific class of small RNAs produced by the germline during meiosis, the scnRNAs, are involved in the epigenetic regulation of DNA deletion but the underlying mechanisms are poorly understood. Here, we show that trimethylation of histone H3 (H3K27me3 and H3K9me3) displays a dynamic nuclear localization that is altered when the endonuclease required for DNA elimination is depleted. We identified the putative histone methyltransferase Ezl1 necessary for H3K27me3 and H3K9me3 establishment and show that it is required for correct genome rearrangements. Genome-wide analyses show that scnRNA-mediated H3 trimethylation is necessary for the elimination of long, repeated germline DNA, while single copy sequences display differential sensitivity to depletion of proteins involved in the scnRNA pathway, Ezl1- a putative histone methyltransferase and Dcl5- a protein required for iesRNA biogenesis. Our study reveals cis-acting determinants, such as DNA length, also contribute to the definition of germline sequences to delete. We further show that precise excision of single copy DNA elements, as short as 26 bp, requires Ezl1, suggesting that development specific H3K27me3 and H3K9me3 ensure specific demarcation of very short germline sequences from the adjacent somatic sequences.
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http://dx.doi.org/10.1371/journal.pgen.1004665DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4177680PMC
September 2014

The Capsaspora genome reveals a complex unicellular prehistory of animals.

Nat Commun 2013 ;4:2325

Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.

To reconstruct the evolutionary origin of multicellular animals from their unicellular ancestors, the genome sequences of diverse unicellular relatives are essential. However, only the genome of the choanoflagellate Monosiga brevicollis has been reported to date. Here we completely sequence the genome of the filasterean Capsaspora owczarzaki, the closest known unicellular relative of metazoans besides choanoflagellates. Analyses of this genome alter our understanding of the molecular complexity of metazoans' unicellular ancestors showing that they had a richer repertoire of proteins involved in cell adhesion and transcriptional regulation than previously inferred only with the choanoflagellate genome. Some of these proteins were secondarily lost in choanoflagellates. In contrast, most intercellular signalling systems controlling development evolved later concomitant with the emergence of the first metazoans. We propose that the acquisition of these metazoan-specific developmental systems and the co-option of pre-existing genes drove the evolutionary transition from unicellular protists to metazoans.
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http://dx.doi.org/10.1038/ncomms3325DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3753549PMC
April 2014

Posterior elongation in the annelid Platynereis dumerilii involves stem cells molecularly related to primordial germ cells.

Dev Biol 2013 Oct 25;382(1):246-67. Epub 2013 Jul 25.

Institut Jacques Monod, CNRS, UMR 7592, Univ Paris Diderot, Sorbonne Paris Cité, F-75205 Paris, France. Electronic address:

Like most bilaterian animals, the annelid Platynereis dumerilii generates the majority of its body axis in an anterior to posterior temporal progression with new segments added sequentially. This process relies on a posterior subterminal proliferative body region, known as the "segment addition zone" (SAZ). We explored some of the molecular and cellular aspects of posterior elongation in Platynereis, in particular to test the hypothesis that the SAZ contains a specific set of stem cells dedicated to posterior elongation. We cloned and characterized the developmental expression patterns of orthologs of 17 genes known to be involved in the formation, behavior, or maintenance of stem cells in other metazoan models. These genes encode RNA-binding proteins (e.g., tudor, musashi, pumilio) or transcription factors (e.g., myc, id, runx) widely conserved in eumetazoans. Most of these genes are expressed both in the migrating primordial germ cells and in overlapping ring-like patterns in the SAZ, similar to some previously analyzed genes (piwi, vasa). The SAZ patterns are coincident with the expression of proliferation markers cyclin B and PCNA. EdU pulse and chase experiments suggest that new segments are produced through many rounds of divisions from small populations of teloblast-like posterior stem cells. The shared molecular signature between primordial germ cells and posterior stem cells in Platynereis thus corresponds to an ancestral "stemness" program.
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http://dx.doi.org/10.1016/j.ydbio.2013.07.013DOI Listing
October 2013

Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii.

Nat Commun 2013 ;4:1915

Institut Jacques Monod, CNRS, UMR 7592, Univ Paris Diderot, Sorbonne Paris Cité, F-75205 Paris, France.

Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/β-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/β-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/β-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.
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http://dx.doi.org/10.1038/ncomms2915DOI Listing
December 2013

Expanding roles for the evolutionarily conserved Dmrt sex transcriptional regulators during embryogenesis.

Cell Mol Life Sci 2013 Oct 5;70(20):3829-45. Epub 2013 Mar 5.

Laboratoire de Génétique du Développement, Institut de Biologie et de Médecine Moléculaires (IBMM), Université Libre de Bruxelles, rue des Profs. Jeener et Brachet 12, 6041, Gosselies, Belgium,

Dmrt genes encode a large family of transcription factors characterized by the presence of a DM domain, an unusual zinc finger DNA binding domain. While Dmrt genes are well known for their important role in sexual development in arthropodes, nematodes and vertebrates, several new findings indicate emerging functions of this gene family in other developmental processes. Here, we provide an overview of the evolution, structure and mechanisms of action of Dmrt genes. We summarize recent findings on their function in sexual regulation and discuss more extensively the role played by these proteins in somitogenesis and neural development.
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http://dx.doi.org/10.1007/s00018-013-1288-2DOI Listing
October 2013

Coe genes are expressed in differentiating neurons in the central nervous system of protostomes.

PLoS One 2011 17;6(6):e21213. Epub 2011 Jun 17.

University of Paris Diderot, Sorbonne Paris Cité, Institut Jacques Monod, UMR 7592 CNRS, Paris, France.

Genes of the coe (collier/olfactory/early B-cell factor) family encode Helix-Loop-Helix transcription factors that are widely conserved in metazoans and involved in many developmental processes, neurogenesis in particular. Whereas their functions during vertebrate neural tube formation have been well documented, very little is known about their expression and role during central nervous system (CNS) development in protostomes. Here we characterized the CNS expression of coe genes in the insect Drosophila melanogaster and the polychaete annelid Platynereis dumerilii, which belong to different subgroups of protostomes and show strikingly different modes of development. In the Drosophila ventral nerve cord, we found that the Collier-expressing cells form a subpopulation of interneurons with diverse molecular identities and neurotransmitter phenotypes. We also demonstrate that collier is required for the proper differentiation of some interneurons belonging to the Eve-Lateral cluster. In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells. Using an original technique of in silico 3D registration, we show that Pdu-coe is co-expressed with many different neuronal markers and therefore that, like in Drosophila, its expression defines a heterogeneous population of neurons with diverse molecular identities. Our detailed characterization and comparison of coe gene expression in the CNS of two distantly-related protostomes suggest conserved roles of coe genes in neuronal differentiation in this clade. As similar roles have also been observed in vertebrates, this function was probably already established in the last common ancestor of all bilaterians.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0021213PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3117877PMC
October 2011

Evolution of RNA-binding proteins in animals: insights from genome-wide analysis in the sponge Amphimedon queenslandica.

Mol Biol Evol 2011 Aug 15;28(8):2289-303. Epub 2011 Feb 15.

Development and Neurobiology Programme, Institut Jacques Monod, Centre national de la recherche scientifique/Université Paris Diderot-Paris 7, Paris cedex, France.

RNA-binding proteins (RBPs) are key players in various biological processes, most notably regulation of gene expression at the posttranscriptional level. Although many RBPs have been carefully studied in model organisms, very few studies have addressed the evolution of these proteins at the scale of the animal kingdom. We identified a large set of putative RBPs encoded by the genome of the demosponge Amphimedon queenslandica, a species representing a basal animal lineage. We compared the Amphimedon RBPs with those encoded by the genomes of two bilaterians (human and Drosophila), representatives of two other basal metazoan lineages (a placozoan and a cnidarian), a choanoflagellate (probable sister group of animals), and two fungi. We established the evolutionary history of 32 families of RBPs and found that most of the diversity of RBPs present in contemporary metazoans, including humans, was already established in the last common ancestor (LCA) of animals. This includes RBPs known to be involved in key processes in bilaterians, such as development, stem and/or germ cells properties, and noncoding RNA pathways. From this analysis, we infer that a complex toolkit of RBPs was present in the LCA of animals and that it has been recruited to perform new functions during early animal evolution, in particular in relation to the acquisition of multicellularity.
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http://dx.doi.org/10.1093/molbev/msr046DOI Listing
August 2011

Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation.

BMC Evol Biol 2010 Dec 1;10:374. Epub 2010 Dec 1.

Department of Earth Sciences, Palaeobiology, Villavägen 16, SE-75236 Uppsala, Sweden.

Background: The Wnt genes encode secreted glycoprotein ligands that regulate a wide range of developmental processes, including axis elongation and segmentation. There are thirteen subfamilies of Wnt genes in metazoans and this gene diversity appeared early in animal evolution. The loss of Wnt subfamilies appears to be common in insects, but little is known about the Wnt repertoire in other arthropods, and moreover the expression and function of these genes have only been investigated in a few protostomes outside the relatively Wnt-poor model species Drosophila melanogaster and Caenorhabditis elegans. To investigate the evolution of this important gene family more broadly in protostomes, we surveyed the Wnt gene diversity in the crustacean Daphnia pulex, the chelicerates Ixodes scapularis and Achaearanea tepidariorum, the myriapod Glomeris marginata and the annelid Platynereis dumerilii. We also characterised Wnt gene expression in the latter three species, and further investigated expression of these genes in the beetle Tribolium castaneum.

Results: We found that Daphnia and Platynereis both contain twelve Wnt subfamilies demonstrating that the common ancestors of arthropods, ecdysozoans and protostomes possessed all members of all Wnt subfamilies except Wnt3. Furthermore, although there is striking loss of Wnt genes in insects, other arthropods have maintained greater Wnt gene diversity. The expression of many Wnt genes overlap in segmentally reiterated patterns and in the segment addition zone, and while these patterns can be relatively conserved among arthropods and the annelid, there have also been changes in the expression of some Wnt genes in the course of protostome evolution. Nevertheless, our results strongly support the parasegment as the primary segmental unit in arthropods, and suggest further similarities between segmental and parasegmental regulation by Wnt genes in annelids and arthropods respectively.

Conclusions: Despite frequent losses of Wnt gene subfamilies in lineages such as insects, nematodes and leeches, most protostomes have probably maintained much of their ancestral repertoire of twelve Wnt genes. The maintenance of a large set of these ligands could be in part due to their combinatorial activity in various tissues rather than functional redundancy. The activity of such Wnt 'landscapes' as opposed to the function of individual ligands could explain the patterns of conservation and redeployment of these genes in important developmental processes across metazoans. This requires further analysis of the expression and function of these genes in a wider range of taxa.
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http://dx.doi.org/10.1186/1471-2148-10-374DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3003278PMC
December 2010

The Amphimedon queenslandica genome and the evolution of animal complexity.

Nature 2010 Aug;466(7307):720-6

Center for Integrative Genomics and Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.

Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
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http://dx.doi.org/10.1038/nature09201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3130542PMC
August 2010

Hedgehog signaling regulates segment formation in the annelid Platynereis.

Science 2010 Jul;329(5989):339-42

Centre de Génétique Moléculaire du CNRS, FRE 3144, Avenue de la Terrasse, 91189 Gif-sur-Yvette, France.

Annelids and arthropods share a similar segmented organization of the body whose evolutionary origin remains unclear. The Hedgehog signaling pathway, prominent in arthropod embryonic segment patterning, has not been shown to have a similar function outside arthropods. We show that the ligand Hedgehog, the receptor Patched, and the transcription factor Gli are all expressed in striped patterns before the morphological appearance of segments in the annelid Platynereis dumerilii. Treatments with small molecules antagonistic to Hedgehog signaling disrupt segment formation. Platynereis Hedgehog is not necessary to establish early segment patterns but is required to maintain them. The molecular similarity of segment patterning functions of the Hedgehog pathway in an annelid and in arthropods supports a common origin of segmentation in protostomes.
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http://dx.doi.org/10.1126/science.1188913DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3182550PMC
July 2010

A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution.

BMC Evol Biol 2010 Mar 11;10:73. Epub 2010 Mar 11.

Laboratoire de Bioinformatique des Génomes et des Réseaux, Université Libre de Bruxelles, Campus Plaine, CP 263, Boulevard du Triomphe, B-1050 Bruxelles, Belgium.

Background: Hox and the closely-related ParaHox genes, which emerged prior to the divergence between cnidarians and bilaterians, are the most well-known members of the ancient genetic toolkit that controls embryonic development across all metazoans. Fundamental questions relative to their origin and evolutionary relationships remain however unresolved. We investigate here the evolution of metazoan Hox and ParaHox genes using the HoxPred program that allows the identification of Hox genes without the need of phylogenetic tree reconstructions.

Results: We show that HoxPred provides an efficient and accurate classification of Hox and ParaHox genes in their respective homology groups, including Hox paralogous groups (PGs). We analyzed more than 10,000 sequences from 310 metazoan species, from 6 genome projects and the complete UniProtKB database. The HoxPred program and all results arranged in the Datab'Hox database are freely available at http://cege.vub.ac.be/hoxpred/. Results for the genome-scale studies are coherent with previous studies, and also brings knowledge on the Hox repertoire and clusters for newly-sequenced species. The unprecedented scale of this study and the use of a non-tree-based approach allows unresolved key questions about Hox and ParaHox genes evolution to be addressed.

Conclusions: Our analysis suggests that the presence of a single type of Posterior Hox genes (PG9-like) is ancestral to bilaterians, and that new Posterior PGs would have arisen in deuterostomes through independent gene duplications. Four types of Central genes would also be ancestral to bilaterians, with two of them, PG6- and PG7-like that gave rise, in protostomes, to the UbdA- and ftz/Antp/Lox5-type genes, respectively. A fifth type of Central genes (PG8) would have emerged in the vertebrate lineage. Our results also suggest the presence of Anterior (PG1 and PG3), Central and Posterior Hox genes in the cnidarians, supporting an ancestral four-gene Hox cluster. In addition, our data support the relationship of the bilaterian ParaHox genes Gsx and Xlox with PG3, and Cdx with the Central genes. Our study therefore indicates three possible models for the origin of Hox and ParaHox in early metazoans, a two-gene (Anterior/PG3--Central/Posterior), a three-gene (Anterior/PG1, Anterior/PG3 and Central/Posterior), or a four-gene (Anterior/PG1--Anterior/PG3--Central--Posterior) ProtoHox cluster.
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http://dx.doi.org/10.1186/1471-2148-10-73DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2842273PMC
March 2010

Early evolution of metazoan transcription factors.

Curr Opin Genet Dev 2009 Dec 31;19(6):591-9. Epub 2009 Oct 31.

School of Biological Sciences, University of Queensland, Brisbane, QLD 4072, Australia.

Analyses of recently sequenced sponge, cnidarian, placozoan, and choanoflagellate genomes have revealed that most transcription factor (TF) classes and families expressed during bilaterian development originated at the dawn of the animal kingdom, before the divergence of contemporary animal lineages. The ancestral metazoan genome included members of the bHLH, Mef2, Fox, Sox, T-box, ETS, nuclear receptor, Rel/NF-kappaB, bZIP, and Smad families, and a diversity of homeobox-containing classes, including ANTP, Prd-like, Pax, POU, LIM-HD, Six, and TALE. As many of these TF classes and families appear to be metazoan specific and not present in choanoflagellates, fungi and more distant eukaryotes, their genesis and expansion may have contributed to the evolution of animal multicellularity.
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http://dx.doi.org/10.1016/j.gde.2009.09.008DOI Listing
December 2009

Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes.

BMC Evol Biol 2009 Oct 13;9:249. Epub 2009 Oct 13.

Aix-Marseille Universités, Centre d'Océanologie de Marseille, Station marine d'Endoume - CNRS UMR 6540-DIMAR, rue de Batterie des Lions, 13007 Marseille, France.

Background: Of the 20 or so signal transduction pathways that orchestrate cell-cell interactions in metazoans, seven are involved during development. One of these is the Notch signalling pathway which regulates cellular identity, proliferation, differentiation and apoptosis via the developmental processes of lateral inhibition and boundary induction. In light of this essential role played in metazoan development, we surveyed a wide range of eukaryotic genomes to determine the origin and evolution of the components and auxiliary factors that compose and modulate this pathway.

Results: We searched for 22 components of the Notch pathway in 35 different species that represent 8 major clades of eukaryotes, performed phylogenetic analyses and compared the domain compositions of the two fundamental molecules: the receptor Notch and its ligands Delta/Jagged. We confirm that a Notch pathway, with true receptors and ligands is specific to the Metazoa. This study also sheds light on the deep ancestry of a number of genes involved in this pathway, while other members are revealed to have a more recent origin. The origin of several components can be accounted for by the shuffling of pre-existing protein domains, or via lateral gene transfer. In addition, certain domains have appeared de novo more recently, and can be considered metazoan synapomorphies.

Conclusion: The Notch signalling pathway emerged in Metazoa via a diversity of molecular mechanisms, incorporating both novel and ancient protein domains during eukaryote evolution. Thus, a functional Notch signalling pathway was probably present in Urmetazoa.
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http://dx.doi.org/10.1186/1471-2148-9-249DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2770060PMC
October 2009

Orthologs of key vertebrate neural genes are expressed during neurogenesis in the annelid Platynereis dumerilii.

Evol Dev 2009 Sep-Oct;11(5):513-24

Programme Development and Neurobiology, Institut Jacques Monod, UMR 7592 CNRS/Université Paris Diderot-Paris 7, 75205 Paris Cedex 13, France.

The molecular mechanisms underlying the formation and patterning of the nervous system are relatively poorly understood for lophotrochozoans (like annelids) as compared with ecdysozoans (especially Drosophila) and deuterostomes (especially vertebrates). Therefore, we have undertaken a candidate gene approach to study aspects of neurogenesis in a polychaete annelid Platynereis dumerilii. We determined the spatiotemporal expression for Platynereis orthologs of four genes (SoxB, Churchill, prospero/Prox, and SoxC) known to play key roles in vertebrate neurogenesis. During Platynereis development, SoxB is expressed in the neuroectoderm and its expression switches off when committed neural precursors are formed. Subsequently, Prox is expressed in all differentiating neural precursors in the central and peripheral nervous systems. Finally, SoxC and Churchill are transcribed in patterns consistent with their involvement in neural differentiation. The expression patterns of Platynereis SoxB and Prox closely resemble those in Drosophila and vertebrates--this suggests that orthologs of these genes play similar neurogenic roles in all bilaterians. Whereas Platynereis SoxC, like its vertebrate orthologs, plays a role in neural cell differentiation, related genes in Drosophila do not appear to be involved in neurogenesis. Finally, conversely to Churchill in Platynereis, vertebrate orthologs of this gene are expressed during neuroectoderm formation, but not later during nerve cell differentiation; in the insect lineage, homologs of these genes have been secondarily lost. In spite of such instances of functional divergence or loss, the present study shows conspicuous similarities in the genetic control of neurogenesis among bilaterians. These commonalities suggest that key features of the genetic program for neurogenesis are ancestral to bilaterians.
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http://dx.doi.org/10.1111/j.1525-142X.2009.00359.xDOI Listing
December 2009

Insights into the evolution of the snail superfamily from metazoan wide molecular phylogenies and expression data in annelids.

BMC Evol Biol 2009 May 9;9:94. Epub 2009 May 9.

Programme Development and Neurobiology, Institut Jacques Monod, UMR 7592 CNRS/Université Paris Diderot - Paris 7, 15 rue Hélène Brion, 75205 Paris Cedex 13, France.

Background: An important issue concerning the evolution of duplicated genes is to understand why paralogous genes are retained in a genome even though the most likely fate for a redundant duplicated gene is nonfunctionalization and thereby its elimination. Here we study a complex superfamily generated by gene duplications, the snail related genes that play key roles during animal development. We investigate the evolutionary history of these genes by genomic, phylogenetic, and expression data studies.

Results: We systematically retrieved the full complement of snail related genes in several sequenced genomes. Through phylogenetic analysis, we found that the snail superfamily is composed of three ancestral families, snail, scratchA and scratchB. Analyses of the organization of the encoded proteins point out specific molecular signatures, indicative of functional specificities for Snail, ScratchA and ScratchB proteins. We also report the presence of two snail genes in the annelid Platynereis dumerilii, which have distinct expression patterns in the developing mesoderm, nervous system, and foregut. The combined expression of these two genes is identical to that of two independently duplicated snail genes in another annelid, Capitella spI, but different aspects of the expression patterns are differentially shared among paralogs of Platynereis and Capitella.

Conclusion: Our study indicates that the snail and scratchB families have expanded through multiple independent gene duplications in the different bilaterian lineages, and highlights potential functional diversifications of Snail and ScratchB proteins following duplications, as, in several instances, paralogous proteins in a given species show different domain organizations. Comparisons of the expression pattern domains of the two Platynereis and Capitella snail paralogs provide evidence for independent subfunctionalization events which have occurred in these two species. We propose that the snail related genes may be especially prone to subfunctionalization, and this would explain why the snail superfamily underwent so many independent duplications leading to maintenance of functional paralogs.
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http://dx.doi.org/10.1186/1471-2148-9-94DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2688512PMC
May 2009

Evolutionary history of the iroquois/Irx genes in metazoans.

BMC Evol Biol 2009 Apr 15;9:74. Epub 2009 Apr 15.

Evolution et Développement des métazoaires, Centre de Génétique Moléculaire - FRE 3144 CNRS, 1, av, de la terrasse, 91198 Gif-sur-Yvette, France.

Background: The iroquois (iro/Irx) genes encode transcriptional regulators that belong to the TALE superclass of homeodomain proteins and have key functions during development in both vertebrates and insects. The Irx genes occur in one or two genomic clusters containing three genes each within the Drosophila and several vertebrate genomes, respectively. The similar genomic organization in Drosophila and vertebrates is widely considered as a result of convergent evolution, due to independent tandem gene duplications. In this study, we investigate the evolutionary history of the Irx genes at the scale of the whole metazoan kingdom.

Results: We identified in silico the putative full complement of Irx genes in the sequenced genomes of 36 different species representative of the main metazoan lineages, including non bilaterian species, several arthropods, non vertebrate chordates, and a basal vertebrate, the sea lamprey. We performed extensive phylogenetic analyses of the identified Irx genes and defined their genomic organizations. We found that, in most species, there are several Irx genes, these genes form two to four gene clusters, and the Irx genes are physically linked to a structurally and functionally unrelated gene known as CG10632 in Drosophila.

Conclusion: Three main conclusions can be drawn from our study. First, an Irx cluster composed of two genes, araucan/caupolican and mirror, is ancestral to the crustaceans+insects clade and has been strongly conserved in this clade. Second, three Irx genes were probably present in the last common ancestor of vertebrates and the duplication that has given rise to the six genes organized into two clusters found in most vertebrates, likely occurred in the gnathostome lineage after its separation from sea lampreys. Third, the clustered organization of the Irx genes in various evolutionary lineages may represent an exceptional case of convergent evolution or may point to the existence of an Irx gene cluster ancestral to bilaterians.
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http://dx.doi.org/10.1186/1471-2148-9-74DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2674049PMC
April 2009

Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit.

Curr Biol 2008 Aug;18(15):1156-61

School of Integrative Biology, University of Queensland, Brisbane, Australia.

The nerve cell is a eumetazoan (cnidarians and bilaterians) synapomorphy [1]; this cell type is absent in sponges, a more ancient phyletic lineage. Here, we demonstrate that despite lacking neurons, the sponge Amphimedon queenslandica expresses the Notch-Delta signaling system and a proneural basic helix loop helix (bHLH) gene in a manner that resembles the conserved molecular mechanisms of primary neurogenesis in bilaterians. During Amphimedon development, a field of subepithelial cells expresses the Notch receptor, its ligand Delta, and a sponge bHLH gene, AmqbHLH1. Cells that migrate out of this field express AmqDelta1 and give rise to putative sensory cells that populate the larval epithelium. Phylogenetic analysis suggests that AmqbHLH1 is descendent from a single ancestral bHLH gene that later duplicated to produce the atonal/neurogenin-related bHLH gene families, which include most bilaterian proneural genes [2]. By way of functional studies in Xenopus and Drosophila, we demonstrate that AmqbHLH1 has a strong proneural activity in both species with properties displayed by both neurogenin and atonal genes. From these results, we infer that the bilaterian neurogenic circuit, comprising proneural atonal-related bHLH genes coupled with Notch-Delta signaling, was functional in the very first metazoans and was used to generate an ancient sensory cell type.
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http://dx.doi.org/10.1016/j.cub.2008.06.074DOI Listing
August 2008

atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes.

BMC Evol Biol 2008 Jun 9;8:170. Epub 2008 Jun 9.

Evolution et Développement des métazoaires, Centre de Génétique Moléculaire-UPR 2167 CNRS, 1, av. de terrasse, 91198 Gif-sur-Yvette, France.

Background: Functional studies in model organisms, such as vertebrates and Drosophila, have shown that basic Helix-loop-Helix (bHLH) proteins have important roles in different steps of neurogenesis, from the acquisition of neural fate to the differentiation into specific neural cell types. However, these studies highlighted many differences in the expression and function of orthologous bHLH proteins during neural development between vertebrates and Drosophila. To understand how the functions of neural bHLH genes have evolved among bilaterians, we have performed a detailed study of bHLH genes during nervous system development in the polychaete annelid, Platynereis dumerilii, an organism which is evolutionary distant from both Drosophila and vertebrates.

Results: We have studied Platynereis orthologs of the most important vertebrate neural bHLH genes, i.e. achaete-scute, neurogenin, atonal, olig, and NeuroD genes, the latter two being genes absent of the Drosophila genome. We observed that all these genes have specific expression patterns during nervous system formation in Platynereis. Our data suggest that in Platynereis, like in vertebrates but unlike Drosophila, (i) neurogenin is the main proneural gene for the formation of the trunk central nervous system, (ii) achaete-scute and olig genes are involved in neural subtype specification in the central nervous system, in particular in the specification of the serotonergic phenotype. In addition, we found that the Platynereis NeuroD gene has a broad and early neuroectodermal expression, which is completely different from the neuronal expression of vertebrate NeuroD genes.

Conclusion: Our analysis suggests that the Platynereis bHLH genes have both proneural and neuronal specification functions, in a way more akin to the vertebrate situation than to that of Drosophila. We conclude that these features are ancestral to bilaterians and have been conserved in the vertebrates and annelids lineages, but have diverged in the evolutionary lineage leading to Drosophila.
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http://dx.doi.org/10.1186/1471-2148-8-170DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2435551PMC
June 2008

The genome of the model beetle and pest Tribolium castaneum.

Nature 2008 Apr 23;452(7190):949-55. Epub 2008 Mar 23.

Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.

Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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http://dx.doi.org/10.1038/nature06784DOI Listing
April 2008

Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis.

Dev Biol 2008 May 21;317(2):430-43. Epub 2008 Feb 21.

Centre de Génétique Moléculaire, CNRS UPR 2167, 1 avenue de la terrasse, 91198 Gif-sur-Yvette, France.

NK genes are related pan-metazoan homeobox genes. In the fruitfly, NK genes are clustered and involved in patterning various mesodermal derivatives during embryogenesis. It was therefore suggested that the NK cluster emerged in evolution as an ancestral mesodermal patterning cluster. To test this hypothesis, we cloned and analysed the expression patterns of the homologues of NK cluster genes Msx, NK4, NK3, Lbx, Tlx, NK1 and NK5 in the marine annelid Platynereis dumerilii, a representative of trochozoans, the third great branch of bilaterian animals alongside deuterostomes and ecdysozoans. We found that most of these genes are involved, as they are in the fly, in the specification of distinct mesodermal derivatives, notably subsets of muscle precursors. The expression of the homologue of NK4/tinman in the pulsatile dorsal vessel of Platynereis strongly supports the hypothesis that the vertebrate heart derived from a dorsal vessel relocated to a ventral position by D/V axis inversion in a chordate ancestor. Additionally and more surprisingly, NK4, Lbx, Msx, Tlx and NK1 orthologues are expressed in complementary sets of stripes in the ectoderm and/or mesoderm of forming segments, suggesting an involvement in the segment formation process. A potentially ancient role of the NK cluster genes in segment formation, unsuspected from vertebrate and fruitfly studies so far, now deserves to be investigated in other bilaterian species, especially non-insect arthropods and onychophorans.
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http://dx.doi.org/10.1016/j.ydbio.2008.02.013DOI Listing
May 2008

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

BMC Evol Biol 2007 Mar 2;7:33. Epub 2007 Mar 2.

Evolution et Développement des protostomiens, Centre de Génétique Moléculaire- UPR 2167 CNRS, Gif-sur-Yvette Cedex, France.

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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http://dx.doi.org/10.1186/1471-2148-7-33DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1828162PMC
March 2007