To Be or Not to Be a Flatworm: The Acoel Controversy
Publication Date
May 11, 2009
Journal
PLOS ONE
Authors
Bernhard Egger, Dirk Steinke, Hiroshi Tarui, Katrien De Mulder, et al
Volume
4
Issue
5
Pages
e5502
DOI
http://doi.org/10.1371/journal.pone.0005502
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0005502
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19430533
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2676513
Europe PMC
http://europepmc.org/abstract/MED/19430533
Web of Science
000266009700007
Scopus
65549158139
Mendeley
http://www.mendeley.com/research/not-flatworm-acoel-controversy
Events
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Mendeley | Further Information

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However, no clear synapomorphies among the three large flatworm taxa -- the Catenulida, the Acoelomorpha and the Rhabditophora -- have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. 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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/899052"], "description"=>"<p>Localization of BrdU-containing cells in the rhabditophorans <i>Prosthiostomum siphunculus</i>, <i>Pseudostylochus intermedius</i>, <i>Planocera reticulata</i> (A–C, Polycladida) and <i>Macrostomum spirale</i> (D, Macrostomorpha). (A) Anterior part of an adult, (B–D) juveniles. Insets: details of the epidermis, encompassed by dotted lines. Anterior to the left. (A–B, D) Note the lack of S-phase cells (brown or green nuclei) in the epidermis after 30 min or 12 h (in B) BrdU pulse. (A) Lower inset shows the protruding pharynx also lacking proliferating cells. (C) BrdU-labeled cells (green nuclei) migrated from the mesodermal space to the epidermis and differentiated into epidermal cells during the 7 days chase period. Scale bar is 50 µm for (D), 100 µm for (B), 400 µm for (C) and 1 mm for (A).</p>", "links"=>[], "tags"=>["proliferation", "rhabditophoran"], "article_id"=>569472, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g003", "stats"=>{"downloads"=>2, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_proliferation_and_cell_migration_in_rhabditophoran_flatworms_/569472", "title"=>"Cell proliferation and cell migration in rhabditophoran flatworms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 02:37:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/899299"], "description"=>"<p>Localization of BrdU-containing cells in the annelid <i>Dorvillea bermudensis</i> (A–C) and the nemertean <i>Cephalothrix</i> sp. (D–E) after 30 min incubation of BrdU. (A) Wholemount of the posterior segments of <i>D. bermudensis</i>. (B) Semithin cross section through midbody and parapodia of animal shown in (A). Labeled cells are located in the epidermis, the mesodermal space, and the gastrodermis (indicated by asterisk). (C) Magnified view of labeled epidermal cells shown in (B). (D) Anterior end of <i>Cephalothrix</i> sp. Labeled cells in the epidermis are separated from muscular layers and the cutis by a light-brown basal matrix. Labeled cells are also present in the mesodermal space. Inset shows details of labeled epidermal cells. (E) More posterior part of the animal than (D) with labeled cells in the epidermis. Arrowheads denote the proboscis. Scale bar is 100 µm for (A), 20 µm for (B), 5 µm for (C), and 50 µm for (D–E).</p>", "links"=>[], "tags"=>["proliferation", "annelid"], "article_id"=>569722, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g004", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_proliferation_in_other_spiralians_an_annelid_and_a_nemertean_/569722", "title"=>"Cell proliferation in other spiralians: an annelid and a nemertean.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 02:42:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/898822"], "description"=>"<p>Localization of BrdU-containing cells in the acoels <i>Isodiametra pulchra</i>, <i>Neochildia fusca</i> and <i>Aphanostoma</i> sp. after a short BrdU pulse (A–B, E–F, H) and 10 days chase (C–D, G). (A, C, E, G–H) wholemounts of adult animals, (B, D, F) semithin cross sections. Insets: details of the epidermis, encompassed by dotted lines. Anterior to the left. (A–B, E–F, H) Note the lack of S-phase cells (brown nuclei) in the epidermis after 30 min BrdU pulse. (C–D, G) BrdU-labeled cells (brown nuclei) migrated from the mesodermal space to the epidermis and differentiated into epidermal cells during the 10 days chase period. Asterisk denotes diatom in digestive parenchyma. Scale bar is 50 µm for (B, D, F, H), 100 µm for (A, C), and 200 µm for (E, G).</p>", "links"=>[], "tags"=>["proliferation", "acoel"], "article_id"=>569237, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_proliferation_and_cell_migration_in_acoel_flatworms_/569237", "title"=>"Cell proliferation and cell migration in acoel flatworms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 02:33:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/899534"], "description"=>"<p><i>In situ</i> hybridizations of adult animals. (A) <i>Isodiametra pulchra</i> (Acoela), (B) <i>Macrostomum lignano</i> (Rhabditophora). Expression of <i>piwi</i>-like genes in the germ line and somatic stem cells. Note the lack of <i>Ipiwi1</i> (A) and <i>Macpiwi</i> (B) expression in the epidermis. Insets: details of the epidermis, encompassed by dotted lines. Accession numbers: <i>Ipiwi1</i> AM942741, <i>Macpiwi</i> AM942740. Scale bar is 100 µm.</p>", "links"=>[], "tags"=>["acoel", "rhabditophoran"], "article_id"=>569954, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g005", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Piwi_like_gene_expression_in_an_acoel_and_a_rhabditophoran_flatworm_/569954", "title"=>"<i>Piwi</i>-like gene expression in an acoel and a rhabditophoran flatworm.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 02:45:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/898615"], "description"=>"<p>The acoel <i>Isodiametra pulchra</i> appears as a sister group of the rest of the bilaterians, and not as a member of the Platyhelminthes. Numbers above nodes refer to the maximum likelihood boostraps. Values below nodes represent bootstrap support under CAT. Circled numbers indicate the percentage of individual-loci trees that supported the respective node in the maximum-likelihood analyses of each data-set separately.</p>", "links"=>[], "tags"=>["23", "sequences", "43"], "article_id"=>569053, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_analysis_of_23_animal_species_using_partial_sequences_of_43_genes_/569053", "title"=>"Phylogenetic analysis of 23 animal species using partial sequences of 43 genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 02:30:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/444879", "https://ndownloader.figshare.com/files/444903", "https://ndownloader.figshare.com/files/444934", "https://ndownloader.figshare.com/files/444992", "https://ndownloader.figshare.com/files/445051"], "description"=>"<div><p>Since first described, acoels were considered members of the flatworms (Platyhelminthes). However, no clear synapomorphies among the three large flatworm taxa - the Catenulida, the Acoelomorpha and the Rhabditophora - have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm <em>Isodiametra pulchra</em> at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a <em>piwi</em>-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.</p></div>", "links"=>[], "tags"=>["acoel"], "article_id"=>147659, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0005502.s001", "https://dx.doi.org/10.1371/journal.pone.0005502.s002", "https://dx.doi.org/10.1371/journal.pone.0005502.s003", "https://dx.doi.org/10.1371/journal.pone.0005502.s004", "https://dx.doi.org/10.1371/journal.pone.0005502.s005"], "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/To_Be_or_Not_to_Be_a_Flatworm_The_Acoel_Controversy/147659", "title"=>"To Be or Not to Be a Flatworm: The Acoel Controversy", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-05-11 02:07:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/899665"], "description"=>"<p>(A) Alternative 1: The similar stem-cell system between Acoela and Rhabditophora is a synapomorphy. This scenario requires a single loss of epidermal stem cells. Notably, the observation of mitotic figures in the epidermis of catenulids supports a sister group relationship of the Catenulida to the Acoela and Rhabditophora. (B) Alternative 2a: The similar stem-cell system between Acoela and Rhabditophora is a plesiomorphy in both taxa. This requires the independent gain of stem cells in the epidermis by the Catenulida, the coelomate Spiralia and other Bilateria not shown in the diagram. (C) Alternative 2b: The similar stem-cell system between Acoela and Rhabditophora is a plesiomorphy in Acoela and a convergent character in Rhabditophora. This requires the gain of stem cells in the epidermis in the Spiralia and other Bilateria not shown in the diagram. (D) Alternative 3: The similar stem-cell system between Acoela and Rhabditophora is a convergent character that was independently developed in both Acoela and Rhabditophora.</p>", "links"=>[], "tags"=>["hypotheses", "epidermal"], "article_id"=>570101, "categories"=>["Cell Biology", "Developmental Biology", "Evolutionary Biology"], "users"=>["Bernhard Egger", "Dirk Steinke", "Hiroshi Tarui", "Katrien De Mulder", "Detlev Arendt", "Gaëtan Borgonie", "Noriko Funayama", "Robert Gschwentner", "Volker Hartenstein", "Bert Hobmayer", "Matthew Hooge", "Martina Hrouda", "Sachiko Ishida", "Chiyoko Kobayashi", "Georg Kuales", "Osamu Nishimura", "Daniela Pfister", "Reinhard Rieger", "Willi Salvenmoser", "Julian Smith III", "Ulrich Technau", "Seth Tyler", "Kiyokazu Agata", "Walter Salzburger", "Peter Ladurner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005502.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alternative_hypotheses_of_evolution_of_epidermal_replacement_/570101", "title"=>"Alternative hypotheses of evolution of epidermal replacement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-11 00:01:41"}

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  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
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  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2014", "month"=>"10"}
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  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"16", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
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  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"2"}
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Relative Metric

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