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Mark Q. Martindale - One of the best experts on this subject based on the ideXlab platform.
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Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation
2018Co-Authors: Timothy Dubuc, Thomas B. Stephenson, Amber Q Rock, Mark Q. MartindaleAbstract:Hox gene transcription factors are important regulators of positional identity along the anterior-posterior axis in Bilaterian animals. Cnidarians (e.g. sea anemones, corals and hydroids) are the sister group to the Bilateria and possess genes related to both anterior and central/posterior class Hox genes. We explore the relationship of two opposing Hox genes in the cnidarian, Nematostella vectenesis. This study identifies and ancient link between Hox/Wnt patterning during axis formation and suggests that the primary axis is patterned during blastula formation in anthozoan cnidarians
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Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans
EvoDevo, 2010Co-Authors: Michael J Layden, Kevin Pang, Néva P Meyer, Elaine C Seaver, Mark Q. MartindaleAbstract:Background zic genes are members of the gli/glis/nkl/zic super-family of C2H2 zinc finger (ZF) transcription factors. Homologs of the zic family have been implicated in patterning neural and mesodermal tissues in Bilaterians. Prior to this study, the origin of the metazoan zic gene family was unknown and expression of zic gene homologs during the development of early branching metazoans had not been investigated. Results Phylogenetic analyses of novel zic candidate genes identified a definitive zic homolog in the placozoan Trichoplax adhaerens , two gli/glis/nkl- like genes in the ctenophore Mnemiopsis leidyi , confirmed the presence of three gli/glis/nkl -like genes in Porifera, and confirmed the five previously identified zic genes in the cnidarian Nematostella vectensis . In the cnidarian N. vectensis , zic homologs are expressed in ectoderm and the gastrodermis (a bifunctional endomesoderm), in presumptive and developing tentacles, and in oral and sensory apical tuft ectoderm. The Capitella teleta zic homolog ( Ct-zic ) is detectable in a subset of the developing nervous system, the foregut, and the mesoderm associated with the segmentally repeated chaetae. Lastly, expression of gli and glis homologs in Mnemiopsis . leidyi is detected exclusively in neural cells in floor of the apical organ. Conclusions Based on our analyses, we propose that the zic gene family arose in the common ancestor of the Placozoa, Cnidaria and Bilateria from a gli/glis/nkl -like gene and that both ZOC and ZF-NC domains evolved prior to cnidarian-Bilaterian divergence. We also conclude that zic expression in neural ectoderm and developing neurons is pervasive throughout the Metazoa and likely evolved from neural expression of an ancestral gli/glis/nkl/zic gene. zic expression in Bilaterian mesoderm may be related to the expression in the gastrodermis of a cnidarian-Bilaterian common ancestor.
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acoel development indicates the independent evolution of the Bilaterian mouth and anus
Nature, 2008Co-Authors: Andreas Hejnol, Mark Q. MartindaleAbstract:Most Bilaterian animals have a 'through' gut, with a mouth at one end and an anus at the other. It is commonly believed that in the transition from radial to Bilaterial symmetry, both openings evolved simultaneously by the partial, lateral closure of a slit-like blastopore. This idea is called into question by work on acoel flatworms, primitive Bilaterians with a mouth but no anus. In studies of the acoel Convolutriloba longifissura, Andreas Hejnol and Mark Martindale use molecular markers to show that the its mouth does indeed correspond with a generic mouth, and that molecular markers characteristic of the hind end of the gut cluster at the (blind) end of the body, in a posterior domain associated with a gonopore. This suggests that the anus evolved many times independently, in association with reproductive structures. Most Bilaterian animals have a through gut and it is commonly believed that in the transition from radial to Bilaterial symmetry, both openings evolved simultaneously by the partial, lateral closure of a slit-like blastopore. This idea is called into question by work on acoel flatworms, primitive Bilaterians that have a mouth but no anus. In studies of the acoel Convolutriloba longifissura, molecular markers are used to show that the acoel's mouth does indeed correspond with a mouth, and that molecular markers characteristic of the hind end of the gut cluster around the (blind) end of the body, in a posterior domain associated with a gonopore. Most Bilaterian animals possess a through gut with a separate mouth and anus1. It is commonly believed that during the transition from radial to bilateral symmetry, both openings evolved simultaneously by the lateral closure of a slit-like blastopore1,2,3,4. Molecular phylogenies however, place the acoel flatworms, which have only one opening to their digestive system, as the sister group to all remaining Bilateria5,6,7. To address how this single body opening is related to the mouth and anus of the protostomes and deuterostomes, we studied the expression of genes involved in Bilaterian foregut and hindgut patterning during the development of the acoel Convolutriloba longifissura. Here we show that the genes brachyury and goosecoid are expressed in association with the acoel mouth, suggesting that this single opening is homologous to the mouth of other Bilaterians8. In addition, we find that the genes caudal, orthopedia and brachyury—which are expressed in various Bilaterian hindguts8,9,10—are expressed in a small region at the posterior end of the animal, separated from the anterior oral brachyury-expressing region by a dorsal domain of ectodermal bmp2/4 expression. These results contradict the hypothesis that the Bilaterian mouth and anus evolved simultaneously from a common blastoporal opening, and suggest that a through gut might have evolved independently in different animal lineages.
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the hedgehog gene family of the cnidarian nematostella vectensis and implications for understanding metazoan hedgehog pathway evolution
Developmental Biology, 2008Co-Authors: David Q. Matus, Mark Q. Martindale, Kevin Pang, Craig R Magie, Gerald H ThomsenAbstract:Hedgehog signaling is an important component of cell-cell communication during Bilaterian development, and abnormal Hedgehog signaling contributes to disease and birth defects. Hedgehog genes are composed of a ligand ("hedge") domain and an autocatalytic intein ("hog") domain. Hedgehog (hh) ligands bind to a conserved set of receptors and activate downstream signal transduction pathways terminating with Gli/Ci transcription factors. We have identified five intein-containing genes in the anthozoan cnidarian Nematostella vectensis, two of which (NvHh1 and NvHh2) contain definitive hedgehog ligand domains, suggesting that to date, cnidarians are the earliest branching metazoan phylum to possess definitive Hh orthologs. Expression analysis of NvHh1 and NvHh2, the receptor NvPatched, and a downstream transcription factor NvGli (a Gli3/Ci ortholog) indicate that these genes may have conserved roles in planar and trans-epithelial signaling during gut and germline development, while the three remaining intein-containing genes (NvHint1,2,3) are expressed in a cell-type-specific manner in putative neural precursors. Metazoan intein-containing genes that lack a hh ligand domain have previously only been identified within nematodes. However, we have identified intein-containing genes from both Nematostella and in two newly annotated lophotrochozoan genomes. Phylogenetic analyses suggest that while nematode inteins may be derived from an ancestral true hedgehog gene, the newly identified cnidarian and lophotrochozoan inteins may be orthologous, suggesting that both true hedgehog and hint genes may have been present in the cnidarian-Bilaterian ancestor. Genomic surveys of N. vectensis suggest that most of the components of both protostome and deuterostome Hh signaling pathways are present in anthozoans and that some appear to have been lost in ecdysozoan lineages. Cnidarians possess many Bilaterian cell-cell signaling pathways (Wnt, TGFbeta, FGF, and Hh) that appear to act in concert to pattern tissues along the oral-aboral axis of the polyp. Cnidarians represent a diverse group of animals with a predominantly epithelial body plan, and perhaps selective pressures to pattern epithelia resulted in the ontogeny of the hedgehog pathway in the common ancestor of the Cnidaria and Bilateria.
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Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis.
Journal of experimental zoology. Part B Molecular and developmental evolution, 2007Co-Authors: Maureen E Mazza, Mark Q. Martindale, Kevin Pang, John R FinnertyAbstract:Otx homeodomain transcription factors have been studied in a variety of eumetazoan animals where they have roles in anterior neural development, endomesoderm formation, and the formation of larval ciliated fields. Here, we describe the gene structure and developmental expression of three Otx loci in the starlet sea anemone, Nematostella vectensis (phylum Cnidaria; class Anthozoa). Nematostella's three Otx genes (OtxA, OtxB, and OtxC) are located in a compact genomic cluster spanning 63.6 kb. The homeodomains of all three Otx genes are highly similar to their Bilaterian counterparts, but only OtxB exhibits the conserved WSP motif that is located downstream of the homeodomain in many Otx proteins. The genomic organization, in concert with phylogenetic analyses, indicates that two tandem duplications occurred in the lineage leading to Nematostella some time after the Cnidaria diverged from the Bilateria. In situ hybridization reveals that otx is initially expressed by invaginating mesendodermal cells in the gastrula. Later, each of the three otx paralogs is expressed in three discrete larval body regions: in the endoderm of the foot or physa, in an endodermal ring surrounding the pharynx, and in the ectoderm of the tentacles. These data suggest that a single otx locus had already acquired diverse developmental functions in the cnidarian-Bilaterian ancestor. Furthermore, following two gene duplications in the line leading to Nematostella, there have been only minor alterations in the spatiotemporal expression of the three Otx paralogs. However, the absence of a conserved protein domain in OtxA and OtxC suggests functional evolution of the protein itself.
Andreas Hejnol - One of the best experts on this subject based on the ideXlab platform.
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Convergent evolution of Bilaterian nerve cords
Nature, 2018Co-Authors: José M. Martín-durán, Ulf Jondelius, Kevin Pang, Aina Børve, Henrike Semmler Lê, Anlaug Furu, Johanna Taylor Cannon, Andreas HejnolAbstract:It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of Bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. Here we study representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida to assess the conservation of the dorsoventral nerve cord patterning. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis , whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria. In Bilaterian animals, the final configurations of central nervous systems seem unrelated to neuroectodermal patterning systems, so it is likely that the various architectures of the ventral nerve cords evolved convergently, many times. Bilaterian animals—that is, bilaterally symmetric animals with distinct anterior and posterior ends—are often thought to have evolved from a common ancestor with a medial, ventral nerve cord. Common molecular patterns along the body axes of animals as diverse as fruit flies, annelid worms and humans support this scenario. Andreas Hejnol and colleagues look at the mediolateral neuroectodermal patterning system in a wide range of animals, including Xenoturbella (a basal Bilaterian) and various lophotrochozoans (such as annelids, brachiopods and rotifers). They observe that the final anatomical configurations of the central nervous system are unrelated to the patterning system. They conclude that similar central nervous system architectures are likely to have arisen many independent times across the Bilaterian group—an example of convergent evolution.
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Convergent evolution of Bilaterian nerve cords
Nature, 2017Co-Authors: José M. Martín-durán, Ulf Jondelius, Kevin Pang, Aina Børve, Anlaug Furu, Johanna Taylor Cannon, Andreas HejnolAbstract:It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of Bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. Here we study representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida to assess the conservation of the dorsoventral nerve cord patterning. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis, whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria.
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Evolution, divergence and loss of the Nodal signalling pathway: new data and a synthesis across the Bilateria
The International Journal of Developmental Biology, 2014Co-Authors: Cristina Grande, José M. Martín-durán, Nathan J. Kenny, Marta Truchado-garcia, Andreas HejnolAbstract:Since the discovery that the TGF-? signalling molecule Nodal and its downstream effector Pitx have a parallel role in establishing asymmetry between molluscs and deuterostomes the debate over the degree to which this signalling pathway is conserved across the Bilateria as a whole has been ongoing. Further taxon sampling is critical to understand the evolution and divergence of this signalling pathway in animals. Using genome and transcriptome mining we confirmed the presence of nodal and Pitx in a range of additional animal taxa for which their presence has not yet been described. In situ hybridization was used to show the embryonic expression of these genes in brachiopods and planarians. We show that both nodal and Pitx genes are broadly conserved across the Spiralia, and nodal likely appeared in the Bilaterian stem lineage after the divergence of the Acoelomorpha. Furthermore, both nodal and Pitx mRNA appears to be expressed in an asymmetric fashion in the brachiopod Terebratalia transversa. No evidence for the presence of a Lefty ortholog could be found in the non-deuterostome genomic resources examined. Nodal expression is asymmetric in a number of spiralian lineages, indicating a possible ancestral role of the Nodal/Pitx cascade in the establishment of asymmetries across the Bilateria.
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Mesodermal Gene Expression in the Acoel Isodiametra pulchra Indicates a Low Number of Mesodermal Cell Types and the Endomesodermal Origin of the Gonads
PLOS ONE, 2013Co-Authors: Marta Chiodin, Pedro Martinez, Aina Børve, Peter Ladurner, Eugene Berezikov, Andreas HejnolAbstract:Acoelomorphs are bilaterally symmetric small marine worms that lack a coelom and possess a digestive system with a single opening. Two alternative phylogenetic positions of this group within the animal tree are currently debated. In one view, Acoelomorpha is the sister group to all remaining Bilateria and as such, is a morphologically simple stepping stone in Bilaterian evolution. In the other, the group is a lineage within the Deuterostomia, and therefore, has derived a simple morphology from a more complex ancestor. Acoels and the closely related Nemertodermatida and Xenoturbellida, which together form the Acoelomorpha, possess a very limited number of cell types. To further investigate the diversity and origin of mesodermal cell types we describe the expression pattern of 12 orthologs of Bilaterian mesodermal markers including Six1/2, Twist, FoxC, GATA4/5/6, in the acoel Isodiametra pulchra. All the genes are expressed in stem cells (neoblasts), gonads, and at least subsets of the acoel musculature. Most are expressed in endomesodermal compartments of I. pulchra developing embryos similar to what has been described in cnidarians. Our molecular evidence indicates a very limited number of mesodermal cell types and suggests an endomesodermal origin of the gonads and the stem cell system. We discuss our results in light of the two prevailing phylogenetic positions of Acoelomorpha.
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Deuterostomic Development in the Protostome Priapulus caudatus
Current biology : CB, 2012Co-Authors: José M. Martín-durán, Ralf Janssen, Sofia A. Wennberg, Graham E. Budd, Andreas HejnolAbstract:Summary The fate of the blastopore during development in the Bilaterian ancestor is currently not well understood. In deuterostomes, the blastopore forms the anus, but its fate in protostome groups is variable [1]. This variability, combined with an absence of information from key taxa, hampers the reconstruction of the ancestral developmental mode of the Protostomia and the Bilateria. The blastopore fate of the Bilaterian ancestor plays a crucial role in understanding the transition from radial to bilateral symmetric organisms [2, 3]. Priapulids have a conservative morphology, an abundant Cambrian fossil record, and a phylogenetic position that make them a key group in understanding protostome evolution [4, 5]. Here, we characterize gastrulation and the embryonic expression of genes involved in Bilaterian foregut and hindgut patterning in Priapulus caudatus . We show that the blastopore gives rise to the anus at the vegetal pole and that the hindgut markers brachyury and caudal are expressed in the blastopore and anus, whereas the foregut markers foxA and goosecoid are expressed in the mouth in the animal hemisphere. Thereby, gastrulation in the conservatively evolving protostome P. caudatus follows strictly a deuterostomic pattern. These results are more compatible with a deuterostomic rather than protostomic (blastopore forms the mouth) or amphistomic (mouth and anus are formed simultaneously) mode of development in the last common Bilaterian ancestor.
John R Finnerty - One of the best experts on this subject based on the ideXlab platform.
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Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis.
Journal of experimental zoology. Part B Molecular and developmental evolution, 2007Co-Authors: Maureen E Mazza, Mark Q. Martindale, Kevin Pang, John R FinnertyAbstract:Otx homeodomain transcription factors have been studied in a variety of eumetazoan animals where they have roles in anterior neural development, endomesoderm formation, and the formation of larval ciliated fields. Here, we describe the gene structure and developmental expression of three Otx loci in the starlet sea anemone, Nematostella vectensis (phylum Cnidaria; class Anthozoa). Nematostella's three Otx genes (OtxA, OtxB, and OtxC) are located in a compact genomic cluster spanning 63.6 kb. The homeodomains of all three Otx genes are highly similar to their Bilaterian counterparts, but only OtxB exhibits the conserved WSP motif that is located downstream of the homeodomain in many Otx proteins. The genomic organization, in concert with phylogenetic analyses, indicates that two tandem duplications occurred in the lineage leading to Nematostella some time after the Cnidaria diverged from the Bilateria. In situ hybridization reveals that otx is initially expressed by invaginating mesendodermal cells in the gastrula. Later, each of the three otx paralogs is expressed in three discrete larval body regions: in the endoderm of the foot or physa, in an endodermal ring surrounding the pharynx, and in the ectoderm of the tentacles. These data suggest that a single otx locus had already acquired diverse developmental functions in the cnidarian-Bilaterian ancestor. Furthermore, following two gene duplications in the line leading to Nematostella, there have been only minor alterations in the spatiotemporal expression of the three Otx paralogs. However, the absence of a conserved protein domain in OtxA and OtxC suggests functional evolution of the protein itself.
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investigating the origins of triploblasty mesodermal gene expression in a diploblastic animal the sea anemone nematostella vectensis phylum cnidaria class anthozoa
Development, 2004Co-Authors: Mark Q. Martindale, Kevin Pang, John R FinnertyAbstract:Mesoderm played a crucial role in the radiation of the triploblastic Bilateria, permitting the evolution of larger and more complex body plans than in the diploblastic, non-Bilaterian animals. The sea anemone Nematostella is a non-Bilaterian animal, a member of the phylum Cnidaria. The phylum Cnidaria (sea anemones, corals, hydras and jellyfish) is the likely sister group of the triploblastic Bilateria. Cnidarians are generally regarded as diploblastic animals, possessing endoderm and ectoderm, but lacking mesoderm. To investigate the origin of triploblasty, we studied the developmental expression of seven genes from Nematostella whose Bilaterian homologs are implicated in mesodermal specification and the differentiation of mesodermal cell types (twist, snailA, snailB, forkhead, mef2, a GATA transcription factor and a LIM transcription factor). Except for mef2, the expression of these genes is largely restricted to the endodermal layer, the gastrodermis. mef2 is restricted to the ectoderm. The temporal and spatial expression of these 'mesoderm' genes suggests that they may play a role in germ layer specification. Furthermore, the predominantly endodermal expression of these genes reinforces the hypothesis that the mesoderm and endoderm of triploblastic animals could be derived from the endoderm of a diploblastic ancestor. Alternatively, we consider the possibility that the diploblastic condition of cnidarians is a secondary simplification, derived from an ancestral condition of triploblasty.
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The origins of axial patterning in the metazoa: how old is bilateral symmetry?
The International Journal of Developmental Biology, 2003Co-Authors: John R FinnertyAbstract:Bilateral symmetry is a hallmark of the Bilateria. It is achieved by the intersection of two orthogonal axes of polarity: the anterior-posterior (A-P) axis and the dorsal-ventral (D-V) axis. It is widely thought that bilateral symmetry evolved in the common ancestor of the Bilateria. However, it has long been known that members of the phylum Cnidaria, an outgroup to the Bilateria, also exhibit bilateral symmetry. Recent studies have examined the developmental expression of axial patterning genes in members of the phylum Cnidaria. Hox genes play a conserved role in patterning the A-P axis of Bilaterians. Hox genes are expressed in staggered axial domains along the oral-aboral axis of cnidarians, suggesting that Hox patterning of the primary body axis was already present in the cnidarian-Bilaterian ancestor. Dpp plays a conserved role patterning the D-V axis of Bilaterians. Asymmetric expression of dpp about the directive axis of cnidarians implies that this patterning system is similarly ancient. Taken together, these result imply that bilateral symmetry had already evolved before the Cnidaria diverged from the Bilateria.
Jorge Vieira - One of the best experts on this subject based on the ideXlab platform.
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Multiple independent L-gulonolactone oxidase (GULO) gene losses and vitamin C synthesis reacquisition events in non-Deuterostomian animal species
BMC Evolutionary Biology, 2019Co-Authors: Sílvia F. Henriques, Pedro Duque, Hugo López-fernández, Florentino Fdez-riverola, Miguel Reboiro-jato, Noé Vázquez, Cristina P Vieira, Jorge VieiraAbstract:Background L-ascorbate (Vitamin C) is an important antioxidant and co-factor in eukaryotic cells, and in mammals it is indispensable for brain development and cognitive function. Vertebrates usually become L-ascorbate auxothrophs when the last enzyme of the synthetic pathway, an L-gulonolactone oxidase ( GULO ), is lost. Since Protostomes were until recently thought not to have a GULO gene, they were considered to be auxothrophs for Vitamin C. Results By performing phylogenetic analyses with tens of non-Bilateria and Protostomian genomes, it is shown, that a GULO gene is present in the non-Bilateria Placozoa, Myxozoa (here reported for the first time) and Anthozoa groups, and in Protostomians, in the Araneae family, the Gastropoda class, the Acari subclass (here reported for the first time), and the Priapulida, Annelida (here reported for the first time) and Brachiopoda phyla lineages. GULO is an old gene that predates the separation of Animals and Fungi, although it could be much older. We also show that within Protostomes, GULO has been lost multiple times in large taxonomic groups, namely the Pancrustacea, Nematoda, Platyhelminthes and Bivalvia groups, a pattern similar to that reported for Vertebrate species. Nevertheless, we show that Drosophila melanogaster seems to be capable of synthesizing L-ascorbate, likely through an alternative pathway, as recently reported for Caenorhabditis elegans . Conclusions Non-Bilaterian and Protostomians seem to be able to synthesize Vitamin C either through the conventional animal pathway or an alternative pathway, but in this animal group, not being able to synthesize L-ascorbate seems to be the exception rather than the rule.
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Multiple independent L-gulonolactone oxidase (GULO) gene losses and vitamin C synthesis reacquisition events in non-Deuterostomian animal species
BMC Evolutionary Biology, 2019Co-Authors: Sílvia Henriques, Pedro Duque, Hugo López-fernández, Florentino Fdez-riverola, Miguel Reboiro-jato, Noé Vázquez, Cristina P Vieira, Jorge VieiraAbstract:L-ascorbate (Vitamin C) is an important antioxidant and co-factor in eukaryotic cells, and in mammals it is indispensable for brain development and cognitive function. Vertebrates usually become L-ascorbate auxothrophs when the last enzyme of the synthetic pathway, an L-gulonolactone oxidase (GULO), is lost. Since Protostomes were until recently thought not to have a GULO gene, they were considered to be auxothrophs for Vitamin C. By performing phylogenetic analyses with tens of non-Bilateria and Protostomian genomes, it is shown, that a GULO gene is present in the non-Bilateria Placozoa, Myxozoa (here reported for the first time) and Anthozoa groups, and in Protostomians, in the Araneae family, the Gastropoda class, the Acari subclass (here reported for the first time), and the Priapulida, Annelida (here reported for the first time) and Brachiopoda phyla lineages. GULO is an old gene that predates the separation of Animals and Fungi, although it could be much older. We also show that within Protostomes, GULO has been lost multiple times in large taxonomic groups, namely the Pancrustacea, Nematoda, Platyhelminthes and Bivalvia groups, a pattern similar to that reported for Vertebrate species. Nevertheless, we show that Drosophila melanogaster seems to be capable of synthesizing L-ascorbate, likely through an alternative pathway, as recently reported for Caenorhabditis elegans. Non-Bilaterian and Protostomians seem to be able to synthesize Vitamin C either through the conventional animal pathway or an alternative pathway, but in this animal group, not being able to synthesize L-ascorbate seems to be the exception rather than the rule.
Kevin Pang - One of the best experts on this subject based on the ideXlab platform.
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Convergent evolution of Bilaterian nerve cords
Nature, 2018Co-Authors: José M. Martín-durán, Ulf Jondelius, Kevin Pang, Aina Børve, Henrike Semmler Lê, Anlaug Furu, Johanna Taylor Cannon, Andreas HejnolAbstract:It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of Bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. Here we study representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida to assess the conservation of the dorsoventral nerve cord patterning. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis , whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria. In Bilaterian animals, the final configurations of central nervous systems seem unrelated to neuroectodermal patterning systems, so it is likely that the various architectures of the ventral nerve cords evolved convergently, many times. Bilaterian animals—that is, bilaterally symmetric animals with distinct anterior and posterior ends—are often thought to have evolved from a common ancestor with a medial, ventral nerve cord. Common molecular patterns along the body axes of animals as diverse as fruit flies, annelid worms and humans support this scenario. Andreas Hejnol and colleagues look at the mediolateral neuroectodermal patterning system in a wide range of animals, including Xenoturbella (a basal Bilaterian) and various lophotrochozoans (such as annelids, brachiopods and rotifers). They observe that the final anatomical configurations of the central nervous system are unrelated to the patterning system. They conclude that similar central nervous system architectures are likely to have arisen many independent times across the Bilaterian group—an example of convergent evolution.
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Convergent evolution of Bilaterian nerve cords
Nature, 2017Co-Authors: José M. Martín-durán, Ulf Jondelius, Kevin Pang, Aina Børve, Anlaug Furu, Johanna Taylor Cannon, Andreas HejnolAbstract:It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of Bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. Here we study representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida to assess the conservation of the dorsoventral nerve cord patterning. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis, whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria.
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Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans
EvoDevo, 2010Co-Authors: Michael J Layden, Kevin Pang, Néva P Meyer, Elaine C Seaver, Mark Q. MartindaleAbstract:Background zic genes are members of the gli/glis/nkl/zic super-family of C2H2 zinc finger (ZF) transcription factors. Homologs of the zic family have been implicated in patterning neural and mesodermal tissues in Bilaterians. Prior to this study, the origin of the metazoan zic gene family was unknown and expression of zic gene homologs during the development of early branching metazoans had not been investigated. Results Phylogenetic analyses of novel zic candidate genes identified a definitive zic homolog in the placozoan Trichoplax adhaerens , two gli/glis/nkl- like genes in the ctenophore Mnemiopsis leidyi , confirmed the presence of three gli/glis/nkl -like genes in Porifera, and confirmed the five previously identified zic genes in the cnidarian Nematostella vectensis . In the cnidarian N. vectensis , zic homologs are expressed in ectoderm and the gastrodermis (a bifunctional endomesoderm), in presumptive and developing tentacles, and in oral and sensory apical tuft ectoderm. The Capitella teleta zic homolog ( Ct-zic ) is detectable in a subset of the developing nervous system, the foregut, and the mesoderm associated with the segmentally repeated chaetae. Lastly, expression of gli and glis homologs in Mnemiopsis . leidyi is detected exclusively in neural cells in floor of the apical organ. Conclusions Based on our analyses, we propose that the zic gene family arose in the common ancestor of the Placozoa, Cnidaria and Bilateria from a gli/glis/nkl -like gene and that both ZOC and ZF-NC domains evolved prior to cnidarian-Bilaterian divergence. We also conclude that zic expression in neural ectoderm and developing neurons is pervasive throughout the Metazoa and likely evolved from neural expression of an ancestral gli/glis/nkl/zic gene. zic expression in Bilaterian mesoderm may be related to the expression in the gastrodermis of a cnidarian-Bilaterian common ancestor.
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the hedgehog gene family of the cnidarian nematostella vectensis and implications for understanding metazoan hedgehog pathway evolution
Developmental Biology, 2008Co-Authors: David Q. Matus, Mark Q. Martindale, Kevin Pang, Craig R Magie, Gerald H ThomsenAbstract:Hedgehog signaling is an important component of cell-cell communication during Bilaterian development, and abnormal Hedgehog signaling contributes to disease and birth defects. Hedgehog genes are composed of a ligand ("hedge") domain and an autocatalytic intein ("hog") domain. Hedgehog (hh) ligands bind to a conserved set of receptors and activate downstream signal transduction pathways terminating with Gli/Ci transcription factors. We have identified five intein-containing genes in the anthozoan cnidarian Nematostella vectensis, two of which (NvHh1 and NvHh2) contain definitive hedgehog ligand domains, suggesting that to date, cnidarians are the earliest branching metazoan phylum to possess definitive Hh orthologs. Expression analysis of NvHh1 and NvHh2, the receptor NvPatched, and a downstream transcription factor NvGli (a Gli3/Ci ortholog) indicate that these genes may have conserved roles in planar and trans-epithelial signaling during gut and germline development, while the three remaining intein-containing genes (NvHint1,2,3) are expressed in a cell-type-specific manner in putative neural precursors. Metazoan intein-containing genes that lack a hh ligand domain have previously only been identified within nematodes. However, we have identified intein-containing genes from both Nematostella and in two newly annotated lophotrochozoan genomes. Phylogenetic analyses suggest that while nematode inteins may be derived from an ancestral true hedgehog gene, the newly identified cnidarian and lophotrochozoan inteins may be orthologous, suggesting that both true hedgehog and hint genes may have been present in the cnidarian-Bilaterian ancestor. Genomic surveys of N. vectensis suggest that most of the components of both protostome and deuterostome Hh signaling pathways are present in anthozoans and that some appear to have been lost in ecdysozoan lineages. Cnidarians possess many Bilaterian cell-cell signaling pathways (Wnt, TGFbeta, FGF, and Hh) that appear to act in concert to pattern tissues along the oral-aboral axis of the polyp. Cnidarians represent a diverse group of animals with a predominantly epithelial body plan, and perhaps selective pressures to pattern epithelia resulted in the ontogeny of the hedgehog pathway in the common ancestor of the Cnidaria and Bilateria.
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Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis.
Journal of experimental zoology. Part B Molecular and developmental evolution, 2007Co-Authors: Maureen E Mazza, Mark Q. Martindale, Kevin Pang, John R FinnertyAbstract:Otx homeodomain transcription factors have been studied in a variety of eumetazoan animals where they have roles in anterior neural development, endomesoderm formation, and the formation of larval ciliated fields. Here, we describe the gene structure and developmental expression of three Otx loci in the starlet sea anemone, Nematostella vectensis (phylum Cnidaria; class Anthozoa). Nematostella's three Otx genes (OtxA, OtxB, and OtxC) are located in a compact genomic cluster spanning 63.6 kb. The homeodomains of all three Otx genes are highly similar to their Bilaterian counterparts, but only OtxB exhibits the conserved WSP motif that is located downstream of the homeodomain in many Otx proteins. The genomic organization, in concert with phylogenetic analyses, indicates that two tandem duplications occurred in the lineage leading to Nematostella some time after the Cnidaria diverged from the Bilateria. In situ hybridization reveals that otx is initially expressed by invaginating mesendodermal cells in the gastrula. Later, each of the three otx paralogs is expressed in three discrete larval body regions: in the endoderm of the foot or physa, in an endodermal ring surrounding the pharynx, and in the ectoderm of the tentacles. These data suggest that a single otx locus had already acquired diverse developmental functions in the cnidarian-Bilaterian ancestor. Furthermore, following two gene duplications in the line leading to Nematostella, there have been only minor alterations in the spatiotemporal expression of the three Otx paralogs. However, the absence of a conserved protein domain in OtxA and OtxC suggests functional evolution of the protein itself.
