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      To Be or Not to Be a Flatworm: The Acoel Controversy

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          Abstract

          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 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. 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.

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          Most cited references44

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          Fundamentals of planarian regeneration.

          The principles underlying regeneration in planarians have been explored for over 100 years through surgical manipulations and cellular observations. Planarian regeneration involves the generation of new tissue at the wound site via cell proliferation (blastema formation), and the remodeling of pre-existing tissues to restore symmetry and proportion (morphallaxis). Because blastemas do not replace all tissues following most types of injuries, both blastema formation and morphallaxis are needed for complete regeneration. Here we discuss a proliferative cell population, the neoblasts, that is central to the regenerative capacities of planarians. Neoblasts may be a totipotent stem-cell population capable of generating essentially every cell type in the adult animal, including themselves. The population properties of the neoblasts and their descendants still await careful elucidation. We identify the types of structures produced by blastemas on a variety of wound surfaces, the principles guiding the reorganization of pre-existing tissues, and the manner in which scale and cell number proportions between body regions are restored during regeneration.
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            SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells.

            We have identified two genes, smedwi-1 and smedwi-2, expressed in the dividing adult stem cells (neoblasts) of the planarian Schmidtea mediterranea. Both genes encode proteins that belong to the Argonaute/PIWI protein family and that share highest homology with those proteins defined by Drosophila PIWI. RNA interference (RNAi) of smedwi-2 blocks regeneration, even though neoblasts are present, irradiation-sensitive, and capable of proliferating in response to wounding; smedwi-2(RNAi) neoblast progeny migrate to sites of cell turnover but, unlike normal cells, fail at replacing aged tissue. We suggest that SMEDWI-2 functions within dividing neoblasts to support the generation of cells that promote regeneration and homeostasis.
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              Biogenesis and germline functions of piRNAs.

              Small interfering RNAs and microRNAs are generated from double-stranded RNA precursors by the Dicer endonucleases, and function with Argonaute-family proteins to target transcript destruction or to silence translation. A distinct class of 24- to 30-nucleotide-long RNAs, produced by a Dicer-independent mechanism, associates with Piwi-class Argonaute proteins. Studies in flies, fish and mice implicate these Piwi-associated RNAs (piRNAs) in germline development, silencing of selfish DNA elements, and in maintaining germline DNA integrity. However, whether piRNAs primarily control chromatin organization, gene transcription, RNA stability or RNA translation is not well understood, neither is piRNA biogenesis. Here, we review recent studies of piRNA production and function, and discuss unanswered questions about this intriguing new class of small RNAs.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2009
                11 May 2009
                : 4
                : 5
                : e5502
                Affiliations
                [1 ]Institute of Zoology and Center for Molecular Biosciences, University of Innsbruck, Innsbruck, Austria
                [2 ]Biodiversity Institute of Ontario, University of Guelph, Guelph, Ontario, Canada
                [3 ]Evolutionary Regeneration Group, Center for Developmental Biology, RIKEN Kobe, Kobe, Japan
                [4 ]Department of Biology, Nematology Section, University of Ghent, Ghent, Belgium
                [5 ]Developmental Biology Programme, EMBL, Heidelberg, Germany
                [6 ]Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, California, United States of America
                [7 ]School of Biology and Ecology, University of Maine, Orono, Maine, United States of America
                [8 ]Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto, Japan
                [9 ]Department of Biofunctional Science, Faculty of Agriculture and Life Sciences, Hirosaki University, Hirosaki, Japan
                [10 ]Division of Integrative Cell Biology, Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto, Japan
                [11 ]Department of Biology, Winthrop University, Rock Hill, South Carolina, United States of America
                [12 ]Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria
                [13 ]Zoological Institute, University of Basel, Basel, Switzerland
                University of Texas Arlington, United States of America
                Author notes

                Conceived and designed the experiments: BE DS HT KDM RR ST KA WS PL. Performed the experiments: BE DS HT KDM RG MH CK GK ON DP WS PL. Analyzed the data: BE DS HT KDM DA GB NF RG VH BH MH MH SI CK GK ON DP RR WS JSI UT ST KA WS PL. Contributed reagents/materials/analysis tools: BE DS HT DA GB NF RG VH BH MH SI JSI UT ST KA WS PL. Wrote the paper: BE DS KDM RR JSI ST KA WS PL.

                Article
                08-PONE-RA-06569R1
                10.1371/journal.pone.0005502
                2676513
                19430533
                87ed3e40-f70a-4a8e-974a-9b5906af2eea
                Egger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 25 September 2008
                : 24 March 2009
                Page count
                Pages: 10
                Categories
                Research Article
                Evolutionary Biology
                Developmental Biology/Cell Differentiation
                Developmental Biology/Developmental Evolution
                Developmental Biology/Stem Cells
                Evolutionary Biology/Developmental Evolution

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                Uncategorized

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