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Andreas Hejnol - One of the best experts on this subject based on the ideXlab platform.
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a single origin of animal excretory organs
bioRxiv, 2020Co-Authors: L Gasiorowski, Ralf Janssen, Graham E. Budd, Carmen Andrikou, P Bump, Christopher J Lowe, Andreas HejnolAbstract:Excretion is an essential physiological process, carried out by all living organisms regardless of their size or complexity(1-3). Most animals, which include both Protostomes (e.g. flies, flatworms) and deuterostomes (e.g. humans, sea urchins) (together Nephrozoa(4, 5)), possess specialized excretory organs. Those organs exhibit an astonishing diversity, ranging from units composed of just three distinct cells (e.g. protonephridia) to complex structures, built by millions of cells of multiple types with divergent morphology and function (e.g. vertebrate kidneys)(6, 7). Although some molecular similarities between the development of kidneys of vertebrates and the regeneration of the protonephridia of flatworms have been reported(8, 9), the molecular development of nephrozoan excretory organs has never been systematically studied in a comparative context(6). Here we show that a set of highly conserved transcription factors and structural proteins is expressed during the development of excretory organs of six species that represent major protostome lineages and non-vertebrate deuterostomes. We demonstrate that the molecular similarity witnessed in the vertebrate kidney and flatworm protonephridia(8) is also seen in the developing excretory organs of other Nephrozoa. In addition, orthologous structural proteins forming the ultrafiltration apparatus are expressed in all these organs in the filter-forming cells. Our results strongly suggest that excretory organs are homologous and are patterned by the conserved set of developmental genes. We propose that the last common nephrozoan ancestor possessed an ultrafiltration-based, ciliated excretory organ, a structure that later gave rise to the vast diversity of extant excretory organs, including the human kidney. Significance statementMost of the bilaterally symmetrical animals excrete through specialized excretory organs, such as kidneys and nephridia. However, due to the morphological diversity of these organs, it remains unknown whether those structures evolved from a common ancestral organ or appeared several times independently during evolution. In order to answer the question about the origin of excretory organs we investigated the molecular pathways and structural genes involved in the development of nephridia in 6 animal species representing major evolutionary lineages. We show that diverse excretory organs share an ancient molecular patterning and structural molecules. Our results provide strong evidence that all excretory organs originated from a single, simple organ that performed urine production by ultrafiltration in deep geological past.
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A nemertean excitatory peptide/CCHamide regulates ciliary swimming in the larvae of Lineus longissimus
Frontiers in Zoology, 2019Co-Authors: Daniel Thiel, Philipp Bauknecht, Gáspár Jékely, Andreas HejnolAbstract:Background The trochozoan excitatory peptide (EP) and its ortholog, the arthropod CCHamide, are neuropeptides that are only investigated in very few animal species. Previous studies on different trochozoan species focused on their physiological effect in adult specimens, demonstrating a myo-excitatory effect, often on tissues of the digestive system. The function of EP in the planktonic larvae of trochozoans has not yet been studied. Results We surveyed transcriptomes from species of various spiralian (Orthonectida, Nemertea, Brachiopoda, Entoprocta, Rotifera) and ecdysozoan taxa (Tardigrada, Onychophora, Priapulida, Loricifera, Nematomorpha) to investigate the evolution of EPs/CCHamides in Protostomes. We found that the EPs of several pilidiophoran nemerteans show a characteristic difference in their C-terminus. Deorphanization of a pilidiophoran EP receptor showed, that the two splice variants of the nemertean Lineus longissimus EP activate a single receptor. We investigated the expression of EP in L. longissimus larvae and juveniles with customized antibodies and found that EP positive nerves in larvae project from the apical organ to the ciliary band and that EP is expressed more broadly in juveniles in the neuropil and the prominent longitudinal nerve cords. While exposing juvenile L. longissimus specimens to synthetic excitatory peptides did not show any obvious effect, exposure of larvae to either of the two EPs increased the beat frequency of their locomotory cilia and shifted their vertical swimming distribution in a water column upwards. Conclusion Our results show that EP/CCHamide peptides are broadly conserved in Protostomes. We show that the EP increases the ciliary beat frequency of L. longissimus larvae, which shifts their vertical distribution in a water column upwards. Endogenous EP may be released at the ciliary band from the projections of apical organ EP positive neurons to regulate ciliary beating. This locomotory function of EP in L. longissimus larvae stands in contrast to the repeated association of EP/CCHamides with its myo-excitatory effect in adult trochozoans and the general association with the digestive system in many Protostomes.
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a nemertean excitatory peptide cchamide regulates ciliary swimming in the larvae of lineus longissimus
Frontiers in Zoology, 2019Co-Authors: Daniel Thiel, Philipp Bauknecht, Gáspár Jékely, Andreas HejnolAbstract:The trochozoan excitatory peptide (EP) and its ortholog, the arthropod CCHamide, are neuropeptides that are only investigated in very few animal species. Previous studies on different trochozoan species focused on their physiological effect in adult specimens, demonstrating a myo-excitatory effect, often on tissues of the digestive system. The function of EP in the planktonic larvae of trochozoans has not yet been studied. We surveyed transcriptomes from species of various spiralian (Orthonectida, Nemertea, Brachiopoda, Entoprocta, Rotifera) and ecdysozoan taxa (Tardigrada, Onychophora, Priapulida, Loricifera, Nematomorpha) to investigate the evolution of EPs/CCHamides in Protostomes. We found that the EPs of several pilidiophoran nemerteans show a characteristic difference in their C-terminus. Deorphanization of a pilidiophoran EP receptor showed, that the two splice variants of the nemertean Lineus longissimus EP activate a single receptor. We investigated the expression of EP in L. longissimus larvae and juveniles with customized antibodies and found that EP positive nerves in larvae project from the apical organ to the ciliary band and that EP is expressed more broadly in juveniles in the neuropil and the prominent longitudinal nerve cords. While exposing juvenile L. longissimus specimens to synthetic excitatory peptides did not show any obvious effect, exposure of larvae to either of the two EPs increased the beat frequency of their locomotory cilia and shifted their vertical swimming distribution in a water column upwards. Our results show that EP/CCHamide peptides are broadly conserved in Protostomes. We show that the EP increases the ciliary beat frequency of L. longissimus larvae, which shifts their vertical distribution in a water column upwards. Endogenous EP may be released at the ciliary band from the projections of apical organ EP positive neurons to regulate ciliary beating. This locomotory function of EP in L. longissimus larvae stands in contrast to the repeated association of EP/CCHamides with its myo-excitatory effect in adult trochozoans and the general association with the digestive system in many Protostomes.
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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.
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gene expression in bryozoan larvae suggest a fundamental importance of pre patterned blastemic cells in the bryozoan life cycle
Evodevo, 2011Co-Authors: Judith Fuchs, Mark Q Martindale, Andreas HejnolAbstract:Bryozoa is a clade of aquatic Protostomes. The bryozoan life cycle typically comprises a larval stage, which metamorphoses into a sessile adult that proliferates by asexual budding to form colonies. The homology of bryozoan larvae with other protostome larvae is enigmatic. Bryozoan larvae exhibit blastemic tissues that contribute to build the adult during morphogenesis. However, it remains unclear if the cells of these tissues are pre-determined according to their future fate or if the cells are undifferentiated, pluripotent stem cells. Gene expression studies can help to identify molecular patterning of larval and adult tissues and enlighten the evolution of bryozoan life cycle stages. We investigated the spatial expression of 13 developmental genes in the larval stage of the gymnolaemate bryozoan Bugula neritina. We found most genes expressed in discrete regions in larval blastemic tissues that form definitive components of the adult body plan. Only two of the 13 genes, BnTropomyosin and BnFoxAB, were exclusively expressed in larval tissues that are discarded during metamorphosis. Our results suggest that the larval blastemas in Bugula are pre-patterned according to their future fate in the adult. The gene expression patterns indicate that some of the bryozoan blastemas can be interpreted to correspond to homologous adult tissues of other animals. This study challenges an earlier proposed view that metazoan larvae share homologous undifferentiated "set-aside cells", and instead points to an independent origin of the bryozoan larval stage with respect to other lophotrochozoans.
Matheus Souza Gomes - One of the best experts on this subject based on the ideXlab platform.
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computational identification and evolutionary relationships of the microrna gene cluster mir 71 2 in Protostomes
Journal of Molecular Evolution, 2013Co-Authors: Matheus Souza Gomes, Mark T. A. Donoghue, Mohankumar Muniyappa, Roberta Verciano Pereira, Renata Guerrasa, Charles SpillaneAbstract:MicroRNAs (miRNAs) are small noncoding RNA molecules which are processed into ~20–24 nt molecules that can regulate the gene expression post-transcriptionally. MiRNA gene clusters have been identified in a range of species, where in miRNAs are often processed from polycistronic transcripts. In this study, a computational approach is used to investigate the extent of evolutionary conservation of the miR-71/2 cluster in animals, and to identify novel miRNAs in the miRNA cluster miR-71/2. The miR-71/2 cluster, consisting of copies of the miR-71 and miR-2 (including miR-13) families, was found to be Protostome-specific. Although, this cluster is highly conserved across the Protostomia, the miR-2 family is completely absent from the Deuterostomia species, while miR-71 is absent from the Vertebrata and Urochordata. The evolutionary conservation and clustering propensity of the miR-71/2 family across the Protostomes could indicate the common functional roles across the member species of the Protostomia.
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Computational Identification and Evolutionary Relationships of the MicroRNA Gene Cluster miR-71/2 in Protostomes
Journal of Molecular Evolution, 2013Co-Authors: Matheus Souza Gomes, Mark T. A. Donoghue, Mohankumar Muniyappa, Roberta Verciano Pereira, Renata Guerra-sá, Charles SpillaneAbstract:MicroRNAs (miRNAs) are small noncoding RNA molecules which are processed into ~20–24 nt molecules that can regulate the gene expression post-transcriptionally. MiRNA gene clusters have been identified in a range of species, where in miRNAs are often processed from polycistronic transcripts. In this study, a computational approach is used to investigate the extent of evolutionary conservation of the miR-71/2 cluster in animals, and to identify novel miRNAs in the miRNA cluster miR-71/2. The miR-71/2 cluster, consisting of copies of the miR-71 and miR-2 (including miR-13) families, was found to be Protostome-specific. Although, this cluster is highly conserved across the Protostomia, the miR-2 family is completely absent from the Deuterostomia species, while miR-71 is absent from the Vertebrata and Urochordata. The evolutionary conservation and clustering propensity of the miR-71/2 family across the Protostomes could indicate the common functional roles across the member species of the Protostomia.
Guillaume Balavoine - One of the best experts on this subject based on the ideXlab platform.
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Extensive Chordate and Annelid Macrosynteny Reveals Ancestral Homeobox Gene Organization.
Molecular Biology and Evolution, 2011Co-Authors: Jerome H L Hui, Detlev Arendt, Guillaume Balavoine, Carmel Mcdougall, Ana S Monteiro, Peter W H Holland, David E K FerrierAbstract:Genes with the homeobox motif are crucial in developmental biology and widely implicated in the evolution of development. The Antennapedia (ANTP)-class is one of the two major classes of animal homeobox genes, and includes the Hox genes, renowned for their role in patterning the anterior-posterior axis of animals. The origin and evolution of the ANTP-class genes are a matter of some debate. A principal guiding hypothesis has been the existence of an ancient gene Mega-cluster deep in animal ancestry. This hypothesis was largely established from linkage data from chordates, and the Mega-cluster hypothesis remains to be seriously tested in Protostomes. We have thus mapped ANTP-class homeobox genes to the chromosome level in a lophotrochozoan protostome. Our comparison of gene organization in Platynereis dumerilii and chordates indicates that the Mega-cluster, if it did exist, had already been broken up onto four chromosomes by the time of the protostome-deuterostome ancestor (PDA). These results not only elucidate an aspect of the genome organization of the PDA but also reveal high levels of macrosynteny between P. dumerilii and chordates. This implies a very low rate of interchromosomal genome rearrangement in the lineages leading to P. dumerilii and the chordate ancestor since the time of the PDA.
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features of the ancestral bilaterian inferred from platynereis dumerilii parahox genes
BMC Biology, 2009Co-Authors: Florian Raible, Claire Jubin, Guillaume Balavoine, Nicolas Dray, Natalia Korchagina, Sylvie Samain, Beatrice Segurens, Ghislaine MagdelenatAbstract:BACKGROUND: The ParaHox gene cluster is the evolutionary sister to the Hox cluster. Whilst the role of the Hox cluster in patterning the anterior-posterior axis of bilaterian animals is well established, and the organisation of vertebrate Hox clusters is intimately linked to gene regulation, much less is known about the more recently discovered ParaHox cluster. ParaHox gene clustering, and its relationship to expression, has only been described in deuterostomes. Conventional protostome models (Drosophila melanogaster and Caenorhabditis elegans) are secondarily derived with respect to ParaHox genes, suffering gene loss and cluster break-up. RESULTS: We provide the first evidence for ParaHox gene clustering from a less-derived protostome animal, the annelid Platynereis dumerilii. Clustering of these genes is thus not a sole preserve of the deuterostome lineage within Bilateria. This protostome ParaHox cluster is not entirely intact however, with Pdu-Cdx being on the opposite end of the same chromosome arm from Pdu-Gsx and Pdu-Xlox. From the genomic sequence around the P. dumerilii ParaHox genes the neighbouring genes are identified, compared with other taxa, and the ancestral arrangement deduced. CONCLUSION: We relate the organisation of the ParaHox genes to their expression, and from comparisons with other taxa hypothesise that a relatively complex pattern of ParaHox gene expression existed in the protostome-deuterostome ancestor, which was secondarily simplified along several invertebrate lineages. Detailed comparisons of the gene content around the ParaHox genes enables the reconstruction of the genome surrounding the ParaHox cluster of the protostome-deuterostome ancestor, which existed over 550 million years ago.
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hox genes in brachiopods and priapulids and protostome evolution
Nature, 1999Co-Authors: Renaud De Rosa, Jennifer K Grenier, Tatiana Andreeva, Charles E Cook, Andre Adoutte, Michael Akam, Sean B Carroll, Guillaume BalavoineAbstract:Understanding the early evolution of animal body plans requires knowledge both of metazoan phylogeny and of the genetic and developmental changes involved in the emergence of particular forms. Recent 18S ribosomal RNA phylogenies suggest a three-branched tree for the Bilateria comprising the deuterostomes and two great protostome clades, the lophotrochozoans1 and ecdysozoans2. Here, we show that the complement of Hox genes in critical protostome phyla reflects these phylogenetic relationships and reveals the early evolution of developmental regulatory potential in bilaterians. We have identified Hox genes that are shared by subsets of protostome phyla. These include a diverged pair of posterior (Abdominal-B -like) genes in both a brachiopod and a polychaete annelid, which supports the lophotrochozoan assemblage, and a distinct posterior Hox gene shared by a priapulid, a nematode and the arthropods, which supports the ecdysozoan clade. The ancestors of each of these two major protostome lineages had a minimum of eight to ten Hox genes. The major period of Hox gene expansion and diversification thus occurred before the radiation of each of the three great bilaterian clades.
Charles Spillane - One of the best experts on this subject based on the ideXlab platform.
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computational identification and evolutionary relationships of the microrna gene cluster mir 71 2 in Protostomes
Journal of Molecular Evolution, 2013Co-Authors: Matheus Souza Gomes, Mark T. A. Donoghue, Mohankumar Muniyappa, Roberta Verciano Pereira, Renata Guerrasa, Charles SpillaneAbstract:MicroRNAs (miRNAs) are small noncoding RNA molecules which are processed into ~20–24 nt molecules that can regulate the gene expression post-transcriptionally. MiRNA gene clusters have been identified in a range of species, where in miRNAs are often processed from polycistronic transcripts. In this study, a computational approach is used to investigate the extent of evolutionary conservation of the miR-71/2 cluster in animals, and to identify novel miRNAs in the miRNA cluster miR-71/2. The miR-71/2 cluster, consisting of copies of the miR-71 and miR-2 (including miR-13) families, was found to be Protostome-specific. Although, this cluster is highly conserved across the Protostomia, the miR-2 family is completely absent from the Deuterostomia species, while miR-71 is absent from the Vertebrata and Urochordata. The evolutionary conservation and clustering propensity of the miR-71/2 family across the Protostomes could indicate the common functional roles across the member species of the Protostomia.
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Computational Identification and Evolutionary Relationships of the MicroRNA Gene Cluster miR-71/2 in Protostomes
Journal of Molecular Evolution, 2013Co-Authors: Matheus Souza Gomes, Mark T. A. Donoghue, Mohankumar Muniyappa, Roberta Verciano Pereira, Renata Guerra-sá, Charles SpillaneAbstract:MicroRNAs (miRNAs) are small noncoding RNA molecules which are processed into ~20–24 nt molecules that can regulate the gene expression post-transcriptionally. MiRNA gene clusters have been identified in a range of species, where in miRNAs are often processed from polycistronic transcripts. In this study, a computational approach is used to investigate the extent of evolutionary conservation of the miR-71/2 cluster in animals, and to identify novel miRNAs in the miRNA cluster miR-71/2. The miR-71/2 cluster, consisting of copies of the miR-71 and miR-2 (including miR-13) families, was found to be Protostome-specific. Although, this cluster is highly conserved across the Protostomia, the miR-2 family is completely absent from the Deuterostomia species, while miR-71 is absent from the Vertebrata and Urochordata. The evolutionary conservation and clustering propensity of the miR-71/2 family across the Protostomes could indicate the common functional roles across the member species of the Protostomia.
David E K Ferrier - One of the best experts on this subject based on the ideXlab platform.
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Another biomineralising protostome with an msp130 gene and conservation of msp130 gene structure across Bilateria
Evolution & development, 2015Co-Authors: Réka Szabó, David E K FerrierAbstract:SUMMARY Msp130 genes are known for their association with biomineralisation, principally in echinoderm skeletogenesis. Recently, msp130 genes were shown to exist more widely across the animal kingdom, including in molluscs, and a hypothesis was formed that the genes had arisen independently in the deuterostome and mollusc lineages via horizontal gene transfer, thus facilitating the evolution of biomineralisation in these distinct lineages (Ettensohn, 2014). Here we show that another biomineralising protostome, the polychaete Spirobranchus (formerly Pomatoceros) lamarcki also possesses an msp130 gene, and expresses it during a biomineralisation process. However, based on analysis of gene structure, we hypothesize that the protostome and deuterostome msp130 genes did not originate from independent horizontal gene transfers, but instead are descended from a gene already present in the bilaterian ancestor, with the gene being secondarily lost from several lineages.
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Evolutionary crossroads in developmental biology: annelids
Development, 2012Co-Authors: David E K FerrierAbstract:Annelids (the segmented worms) have a long history in studies of animal developmental biology, particularly with regards to their cleavage patterns during early development and their neurobiology. With the relatively recent reorganisation of the phylogeny of the animal kingdom, and the distinction of the super-phyla Ecdysozoa and Lophotrochozoa, an extra stimulus for studying this phylum has arisen. As one of the major phyla within Lophotrochozoa, Annelida are playing an important role in deducing the developmental biology of the last common ancestor of the Protostomes and deuterostomes, an animal from which >98% of all described animal species evolved.
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Extensive Chordate and Annelid Macrosynteny Reveals Ancestral Homeobox Gene Organization.
Molecular Biology and Evolution, 2011Co-Authors: Jerome H L Hui, Detlev Arendt, Guillaume Balavoine, Carmel Mcdougall, Ana S Monteiro, Peter W H Holland, David E K FerrierAbstract:Genes with the homeobox motif are crucial in developmental biology and widely implicated in the evolution of development. The Antennapedia (ANTP)-class is one of the two major classes of animal homeobox genes, and includes the Hox genes, renowned for their role in patterning the anterior-posterior axis of animals. The origin and evolution of the ANTP-class genes are a matter of some debate. A principal guiding hypothesis has been the existence of an ancient gene Mega-cluster deep in animal ancestry. This hypothesis was largely established from linkage data from chordates, and the Mega-cluster hypothesis remains to be seriously tested in Protostomes. We have thus mapped ANTP-class homeobox genes to the chromosome level in a lophotrochozoan protostome. Our comparison of gene organization in Platynereis dumerilii and chordates indicates that the Mega-cluster, if it did exist, had already been broken up onto four chromosomes by the time of the protostome-deuterostome ancestor (PDA). These results not only elucidate an aspect of the genome organization of the PDA but also reveal high levels of macrosynteny between P. dumerilii and chordates. This implies a very low rate of interchromosomal genome rearrangement in the lineages leading to P. dumerilii and the chordate ancestor since the time of the PDA.
