Genetic and Genomic Tools for the Marine Annelid Platynereis dumerilii

The bristle worm Platynereis dumerilii displays many interesting biological characteristics. These include its reproductive timing, which is synchronized to the moon phase, its regenerative capacity that is hormonally controlled, and a slow rate of evolution, which permits analyses of ancestral genes and cell types. As a marine annelid, Platynereis is also representative of the marine ecosystem, as well as one of the three large animal subphyla, the Lophotrochozoa. Here, we provide an overview of the molecular resources, functional techniques, and behavioral assays that have recently been established for the bristle worm. This combination of tools now places Platynereis in an excellent position to advance research at the frontiers of neurobiology, chronobiology, evo-devo, and marine biology.

[1]  S Chandrasegaran,et al.  Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  P. Bork,et al.  Vertebrate-Type Intron-Rich Genes in the Marine Annelid Platynereis dumerilii , 2005, Science.

[3]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[4]  Andrew R. Jackson,et al.  The Genome of the Sea Urchin Strongylocentrotus purpuratus , 2006, Science.

[5]  S. Kirchmaier,et al.  Tools for Gene-Regulatory Analyses in the Marine Annelid Platynereis dumerilii , 2014, PloS one.

[6]  J. Keith Joung,et al.  FLASH Assembly of TALENs Enables High-Throughput Genome Editing , 2012, Nature Biotechnology.

[7]  D. Arendt,et al.  Molecular Architecture of Annelid Nerve Cord Supports Common Origin of Nervous System Centralization in Bilateria , 2007, Cell.

[8]  F. Raible,et al.  TALENs Mediate Efficient and Heritable Mutation of Endogenous Genes in the Marine Annelid Platynereis dumerilii , 2014, Genetics.

[9]  Elo Leung,et al.  Targeted Genome Editing Across Species Using ZFNs and TALENs , 2011, Science.

[10]  Xia Li,et al.  High-efficiency and heritable gene targeting in mouse by transcription activator-like effector nucleases , 2013, Nucleic acids research.

[11]  R. P. Kostyuchenko,et al.  Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa) , 2006, Development Genes and Evolution.

[12]  F. Raible,et al.  Conditional and Specific Cell Ablation in the Marine Annelid Platynereis dumerilii , 2013, PloS one.

[13]  C. Barbas,et al.  ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. , 2013, Trends in biotechnology.

[14]  J. Doudna,et al.  A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity , 2012, Science.

[15]  S. Wolfe,et al.  Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleases , 2013, Genome research.

[16]  Daniel F. Voytas,et al.  Simple Methods for Generating and Detecting Locus-Specific Mutations Induced with TALENs in the Zebrafish Genome , 2012, PLoS genetics.

[17]  David A. Scott,et al.  Double Nicking by RNA-Guided CRISPR Cas9 for Enhanced Genome Editing Specificity , 2013, Cell.

[18]  Wei Zhu,et al.  Evolutionary Strategies for the Elucidation ofcisandtransFactors That Regulate the Developmental Switching Programs of the β-like Globin Genes , 1996 .

[19]  C. Ackermann,et al.  Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta) , 2005, Journal of morphology.

[20]  Rudolf Jaenisch,et al.  One-Step Generation of Mice Carrying Mutations in Multiple Genes by CRISPR/Cas-Mediated Genome Engineering , 2013, Cell.

[21]  Bo Zhang,et al.  EENdb: a database and knowledge base of ZFNs and TALENs for endonuclease engineering , 2012, Nucleic Acids Res..

[22]  C. Hauenschild Photoperiodizität als Ursache des von der Mondphase abhängigen Metamorphose-Rhythmus bei dem Polychaeten Platynereis Dumerilii , 1955 .

[23]  Raju Tomer,et al.  Profiling by Image Registration Reveals Common Origin of Annelid Mushroom Bodies and Vertebrate Pallium , 2010, Cell.

[24]  Takahito Watanabe,et al.  Non-transgenic genome modifications in a hemimetabolous insect using zinc-finger and TAL effector nucleases , 2012, Nature Communications.

[25]  George M. Church,et al.  Heritable genome editing in C. elegans via a CRISPR-Cas9 system , 2013, Nature Methods.

[26]  D. Arendt,et al.  Duplication of the ribosomal gene cluster in the marine polychaete Platynereis dumerilii correlates with ITS polymorphism , 2007, Journal of the Marine Biological Association of the United Kingdom.

[27]  M. Vervoort,et al.  Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii , 2013, Nature Communications.

[28]  J. Keith Joung,et al.  Improving CRISPR-Cas nuclease specificity using truncated guide RNAs , 2014, Nature Biotechnology.

[29]  J. Dasen Long noncoding RNAs in development: solidifying the Lncs to Hox gene regulation. , 2013, Cell reports.

[30]  Laser ablation of persistent twist cells in Drosophila: muscle precursor fate is not segmentally restricted. , 1999, Development.

[31]  Thorsten Henrich,et al.  The normal development of Platynereis dumerilii (Nereididae, Annelida) , 2010, Frontiers in Zoology.

[32]  Prashant Mali,et al.  Orthogonal Cas9 Proteins for RNA-Guided Gene Regulation and Editing , 2013, Nature Methods.

[33]  Takashi Yamamoto,et al.  Targeted mutagenesis in sea urchin embryos using TALENs , 2014, Development, growth & differentiation.

[34]  C. Hauenschild Lunar periodicity. , 1960, Cold Spring Harbor symposia on quantitative biology.

[35]  Jeffry D. Sander,et al.  Efficient In Vivo Genome Editing Using RNA-Guided Nucleases , 2013, Nature Biotechnology.

[36]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[37]  James E. DiCarlo,et al.  RNA-Guided Human Genome Engineering via Cas9 , 2013, Science.

[38]  Cori Bargmann,et al.  Laser killing of cells in Caenorhabditis elegans. , 1995, Methods in cell biology.

[39]  D. Arendt,et al.  Arthropod-like Expression Patterns of engrailed and wingless in the Annelid Platynereis dumerilii Suggest a Role in Segment Formation , 2003, Current Biology.

[40]  Elo Leung,et al.  A TALE nuclease architecture for efficient genome editing , 2011, Nature Biotechnology.

[41]  D. Arendt,et al.  Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation , 2007, Proceedings of the National Academy of Sciences.

[42]  An Xiao,et al.  Heritable gene targeting in zebrafish using customized TALENs , 2011, Nature Biotechnology.

[43]  Anton Dohrn Der Ursprung der Wirbelthiere und das Princip des Functionswechsels : Genealogische Skizzen , 1875 .

[44]  H. Hausen,et al.  Conserved Sensory-Neurosecretory Cell Types in Annelid and Fish Forebrain: Insights into Hypothalamus Evolution , 2007, Cell.

[45]  Jens Boch,et al.  Breaking the Code of DNA Binding Specificity of TAL-Type III Effectors , 2009, Science.

[46]  Marilyn Fisher,et al.  Simple and efficient CRISPR/Cas9‐mediated targeted mutagenesis in Xenopus tropicalis , 2013, Genesis.

[47]  S. Tunaru,et al.  Conserved MIP receptor–ligand pair regulates Platynereis larval settlement , 2013, Proceedings of the National Academy of Sciences.

[48]  R. Ketteler,et al.  A CRISPR CASe for high-throughput silencing , 2013, Front. Genet..

[49]  P. Jeggo,et al.  The repair and signaling responses to DNA double-strand breaks. , 2013, Advances in genetics.

[50]  F. Hempelmann Zur Naturgeschichte von Nereis Dumerilii Aud. et Edw. , 1910 .

[51]  D. Arendt,et al.  Is ventral in insects dorsal in vertebrates? , 1994, Roux's archives of developmental biology.

[52]  D. K. Hofmann Regeneration and endocrinology in the polychaetePlatynereis dumerilii , 1976, Wilhelm Roux's archives of developmental biology.

[53]  Erin L. Doyle,et al.  Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting , 2011, Nucleic acids research.

[54]  Oleg Simakov,et al.  Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii. , 2013, Briefings in functional genomics.

[55]  J. Keith Joung,et al.  Improved Somatic Mutagenesis in Zebrafish Using Transcription Activator-Like Effector Nucleases (TALENs) , 2012, PloS one.

[56]  Pierre Kerner,et al.  Orthologs of key vertebrate neural genes are expressed during neurogenesis in the annelid Platynereis dumerilii , 2009, Evolution & development.

[57]  F. Raible,et al.  Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution , 2012, Proceedings of the National Academy of Sciences.

[58]  Awadhesh N. Jha,et al.  The chromosomes Of Platynereis dumerilii (Polychaeta: Nereidae) , 1995, Journal of the Marine Biological Association of the United Kingdom.

[59]  C. Hauenschild Hormonale Hemmung der Geschlechtsreife und Metamorphose bei dem Polychaeten Platynereis Dumerilii , 1956 .

[60]  J. Keith Joung,et al.  High frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells , 2013, Nature Biotechnology.

[61]  H. Hausen,et al.  Mechanism of phototaxis in marine zooplankton , 2008, Nature.

[62]  I. Dawid,et al.  Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs) , 2012, Proceedings of the National Academy of Sciences.

[63]  J. Eisen,et al.  Controlling morpholino experiments: don't stop making antisense , 2008, Development.

[64]  J. Piatigorsky,et al.  Ancestry of Photic and Mechanic Sensation? , 2005, Science.

[65]  T. Münch,et al.  Neuropeptides regulate swimming depth of Platynereis larvae , 2011, Proceedings of the National Academy of Sciences.

[66]  C. Jubin,et al.  Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes , 2009, BMC Biology.

[67]  Ryan M. Anderson,et al.  Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies , 2008, Nature Protocols.

[68]  D. Arendt,et al.  Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain , 2004, Science.

[69]  Sean B. Carroll,et al.  Hox genes in brachiopods and priapulids and protostome evolution , 1999, Nature.

[70]  M. Durchon,et al.  Purification par chromatographie liquide de haute pression (HPLC) de l'hormone cérébrale chez Nereis diversicolor et Perinereis cultrifera (Annélides Polychètes) , 1981 .

[71]  Matthew M. Hill,et al.  Extreme genomic variation in a natural population , 2007, Proceedings of the National Academy of Sciences.

[72]  A. Hassanin Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. , 2006, Molecular Phylogenetics and Evolution.

[73]  D. Arendt,et al.  Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. , 2003, Current opinion in genetics & development.

[74]  Matthew J. Moscou,et al.  A Simple Cipher Governs DNA Recognition by TAL Effectors , 2009, Science.

[75]  E. Lander,et al.  Genetic Screens in Human Cells Using the CRISPR-Cas9 System , 2013, Science.

[76]  E. Naylor,et al.  Chronobiology of Marine Organisms , 2010 .

[77]  T. Shibata,et al.  Targeted mutagenesis in the sea urchin embryo using zinc-finger nucleases , 2010 .

[78]  S. Keplinger Influence of the adult eyes on circadian and lunar rhythms in Platynereis dumerilii , 2010 .

[79]  F. Raible,et al.  Another place, another timer: Marine species and the rhythms of life , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[80]  J. Kadane,et al.  Bayesian phylogenetic inference from animal mitochondrial genome arrangements , 2002 .

[81]  Le Cong,et al.  Multiplex Genome Engineering Using CRISPR/Cas Systems , 2013, Science.

[82]  R. P. Kostyuchenko,et al.  The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii , 2011, Evolution & development.

[83]  T. Todo,et al.  Circadian and Circalunar Clock Interactions in a Marine Annelid , 2013, Cell reports.

[84]  M. Goodman,et al.  Evolutionary strategies for the elucidation of cis and trans factors that regulate the developmental switching programs of the beta-like globin genes. , 1996, Molecular phylogenetics and evolution.

[85]  D. Arendt,et al.  Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development. , 2005, BioTechniques.

[86]  A. Dorresteijn,et al.  Molecular specification of cell lines in the embryo of Platynereis (Annelida) , 1993, Roux's archives of developmental biology.

[87]  D. Arendt,et al.  Hedgehog Signaling Regulates Segment Formation in the Annelid Platynereis , 2010, Science.

[88]  Neville E. Sanjana,et al.  Genome-Scale CRISPR-Cas9 Knockout Screening in Human Cells , 2014, Science.

[89]  S. Bhattacharya,et al.  Site Specific Mutation of the Zic2 Locus by Microinjection of TALEN mRNA in Mouse CD1, C3H and C57BL/6J Oocytes , 2013, PloS one.

[90]  B. Bowerman,et al.  beta-Catenin asymmetries after all animal/vegetal- oriented cell divisions in Platynereis dumerilii embryos mediate binary cell-fate specification. , 2007, Developmental cell.

[91]  Gáspár Jékely,et al.  Cellular resolution expression profiling using confocal detection of NBT/BCIP precipitate by reflection microscopy. , 2007, BioTechniques.

[92]  J. Boore Complete mitochondrial genome sequence of the polychaete annelid Platynereis dumerilii. , 2001, Molecular biology and evolution.

[93]  D. Arendt,et al.  Evolution of the bilaterian larval foregut , 2001, Nature.

[94]  Jeffry D Sander,et al.  FLAsH assembly of TALeNs for high-throughput genome editing , 2022 .

[95]  R. Jiao,et al.  Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. , 2012, Journal of genetics and genomics = Yi chuan xue bao.

[96]  Anton Dohrn,et al.  Der Ursprung der Wirbelthiere und das Princip des Functionswechsels , 2007, Theory in Biosciences.

[97]  Randall J. Platt,et al.  Optical Control of Mammalian Endogenous Transcription and Epigenetic States , 2013, Nature.

[98]  J. Harms Über ein inkretorisches Cerebralorgan bei Lumbriciden, sowie Beschreibung eines verwandten Organs bei drei neuen Lycastis-Arten , 1948, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[99]  D. Arendt,et al.  Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. , 2002, Development.

[100]  G. Church,et al.  CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering , 2013, Nature Biotechnology.

[101]  F. Raible,et al.  17β-Estradiol induces supernumerary primordial germ cells in embryos of the polychaete Platynereis dumerilii. , 2014, General and comparative endocrinology.

[102]  Thomas Gaj,et al.  Expanding the scope of site‐specific recombinases for genetic and metabolic engineering , 2014, Biotechnology and bioengineering.

[103]  A. Dorresteijn,et al.  The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[104]  Steven Lin,et al.  Precise and Heritable Genome Editing in Evolutionarily Diverse Nematodes Using TALENs and CRISPR/Cas9 to Engineer Insertions and Deletions , 2013, Genetics.

[105]  Peer Bork,et al.  Ancient animal microRNAs and the evolution of tissue identity , 2010, Nature.