Development of the annelid axochord: Insights into notochord evolution

Origin of the spine lies in a worm The notochord, the developmental backbone precursor, defines chordates—the group of animals to which humans belong. The origin of the notochord remains mysterious. Lauri et al. report the identification of a longitudinal muscle in an annelid worm that displays striking similarities to the notochord regarding position, developmental origin, and expression profile. Similar muscles, termed axochords, are found in various invertebrate phyla. These data suggest that the last common ancestor of bilaterians already possessed contractile midline tissue that, via stiffening, developed into a cartilaginous rod in the chordate line. Science, this issue p. 1365 A comparative study suggests that the chordate notochord evolved from a ventral midline muscle in bilaterian ancestors. The origin of chordates has been debated for more than a century, with one key issue being the emergence of the notochord. In vertebrates, the notochord develops by convergence and extension of the chordamesoderm, a population of midline cells of unique molecular identity. We identify a population of mesodermal cells in a developing invertebrate, the marine annelid Platynereis dumerilii, that converges and extends toward the midline and expresses a notochord-specific combination of genes. These cells differentiate into a longitudinal muscle, the axochord, that is positioned between central nervous system and axial blood vessel and secretes a strong collagenous extracellular matrix. Ancestral state reconstruction suggests that contractile mesodermal midline cells existed in bilaterian ancestors. We propose that these cells, via vacuolization and stiffening, gave rise to the chordate notochord.

[1]  B. Nickel,et al.  Illuminating the base of the annelid tree using transcriptomics. , 2014, Molecular biology and evolution.

[2]  Raju Tomer,et al.  Larval body patterning and apical organs are conserved in animal evolution , 2014, BMC Biology.

[3]  A. Wanninger,et al.  Aplacophoran Mollusks Evolved from Ancestors with Polyplacophoran-like Features , 2013, Current Biology.

[4]  H. Wada,et al.  Hemichordate neurulation and the origin of the neural tube , 2013, Nature Communications.

[5]  H. Reichert,et al.  A complete three-dimensional reconstruction of the myoanatomy of Loricifera: comparative morphology of an adult and a Higgins larva stage , 2013, Frontiers in Zoology.

[6]  N. Odintsova,et al.  Larval myogenesis in Echinodermata: conserved features and morphological diversity between class‐specific larval forms of Echinoidae, Asteroidea, and Holothuroidea , 2013, Evolution & development.

[7]  Nicholas H. Putnam,et al.  Insights into bilaterian evolution from three spiralian genomes , 2012, Nature.

[8]  T. Cedhagen,et al.  Biology and distribution of hemichordates (Enteropneusta) with emphasis on Harrimaniidae and description of Protoglossus bocki sp. nov. from Scandinavia , 2012, Helgoland Marine Research.

[9]  Philipp J. Keller,et al.  Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy , 2012, Nature Methods.

[10]  K. Tagawa,et al.  How was the notochord born? , 2012, Evolution & development.

[11]  T. Stach,et al.  The central and peripheral nervous system of Cephalodiscus gracilis (Pterobranchia, Deuterostomia) , 2012, Zoomorphology.

[12]  J. Rossant,et al.  Integrated microarray and ChIP analysis identifies multiple Foxa2 dependent target genes in the notochord. , 2011, Developmental biology.

[13]  A. Wanninger,et al.  Cellular and muscular growth patterns during sipunculan development. , 2011, Journal of experimental zoology. Part B, Molecular and developmental evolution.

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

[15]  I. Dawid,et al.  Kctd15 inhibits neural crest formation by attenuating Wnt/β-catenin signaling output , 2010, Development.

[16]  P. Tam,et al.  Loss of procollagen IIA from the anterior mesendoderm disrupts the development of mouse embryonic forebrain , 2010, Developmental dynamics : an official publication of the American Association of Anatomists.

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

[18]  G. Purschke,et al.  Musculature in polychaetes: comparison of Myrianida prolifera (Syllidae) and Sphaerodoropsis sp. (Sphaerodoridae) , 2010 .

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

[20]  A. Wanninger,et al.  Integrative analysis of polychaete ontogeny: cell proliferation patterns and myogenesis in trochophore larvae of Sabellaria alveolata , 2010, Evolution & development.

[21]  M. Boyle,et al.  Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula) , 2010, EvoDevo.

[22]  M. Martindale,et al.  Assessing the root of bilaterian animals with scalable phylogenomic methods , 2009, Proceedings of the Royal Society B: Biological Sciences.

[23]  J. E. Webb The role of the notochard in forward and reverse swimming and burrowing in the amphioxus Branchiostoma lanceolatum , 2009 .

[24]  M. Klymkowsky,et al.  Unexpected functional redundancy between Twist and Slug (Snail2) and their feedback regulation of NF-kappaB via Nodal and Cerberus. , 2009, Developmental biology.

[25]  F. Leasi,et al.  Meiofaunal cryptic species revealed by confocal microscopy: the case of Xenotrichula intermedia (Gastrotricha) , 2009 .

[26]  A. Wanninger,et al.  Three‐dimensional reconstruction of the musculature of various life cycle stages of the cycliophoran Symbion americanus , 2009, Journal of morphology.

[27]  M. Bronner‐Fraser,et al.  Comprehensive spatiotemporal analysis of early chick neural crest network genes , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[28]  A. Wanninger,et al.  Comparative larval myogenesis and adult myoanatomy of the rhynchonelliform (articulate) brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa , 2009, Frontiers in Zoology.

[29]  F. Leasi,et al.  The muscular system of Musellifer delamarei (Renaud-Mornant, 1968) and other chaetonotidans with implications for the phylogeny and systematization of the Paucitubulatina (Gastrotricha) , 2008 .

[30]  P. M. Arbizu,et al.  Organisation of body musculature in Encentrum mucronatum Wulfert, 1936, Dicranophorus forcipatus (O. F. Müller, 1786) and in the ground pattern of Ploima (Rotifera: Monogononta) , 2008 .

[31]  David Q. Matus,et al.  Broad phylogenomic sampling improves resolution of the animal tree of life , 2008, Nature.

[32]  G. Gyapay,et al.  Chætognath transcriptome reveals ancestral and unique features among bilaterians , 2008, Genome Biology.

[33]  G. Scholtz,et al.  Three-dimensional reconstruction of the central nervous system of Macrobiotus hufelandi (Eutardigrada, Parachela): implications for the phylogenetic position of Tardigrada , 2008, Zoomorphology.

[34]  Monika C. M. Müller,et al.  F-actin framework in Spirorbis cf. spirorbis (Annelida: Serpulidae): phalloidin staining investigated and reconstructed by cLSM , 2007 .

[35]  Cheol‐Hee Kim,et al.  Four twist genes in zebrafish, four expression patterns , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[36]  M. Bronner‐Fraser,et al.  Insights from Amphioxus into the Evolution of Vertebrate Cartilage , 2007, PloS one.

[37]  A. Wanninger,et al.  Early development of the aplacophoran mollusc Chaetoderma , 2007 .

[38]  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.

[39]  William C. Smith,et al.  Ascidian notochord morphogenesis , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[40]  Kariena Dill,et al.  Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I , 2007, Development Genes and Evolution.

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

[42]  G. Purschke,et al.  Three-dimensional reconstruction of the F-actin musculature of Dorvillea kastjani (Dorvilleidae, Polychaeta) by means of phalloidin-labelling and cLSM , 2006 .

[43]  D. Kessler,et al.  FoxD3 regulation of Nodal in the Spemann organizer is essential for Xenopus dorsal mesoderm development , 2006, Development.

[44]  J. Gerhart The deuterostome ancestor , 2006, Journal of cellular physiology.

[45]  C. McDougall,et al.  The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes , 2006, Frontiers in Zoology.

[46]  Giorgio F. Gilestro,et al.  Regulation of commissural axon pathfinding by slit and its Robo receptors. , 2006, Annual review of cell and developmental biology.

[47]  J. Weissenbach,et al.  Chaetognath phylogenomics: a protostome with deuterostome-like development , 2006, Current Biology.

[48]  K. Worsaae,et al.  CLSM analysis of the phalloidin‐stained muscle system in Nerilla antennata, Nerillidium sp. and Trochonerilla mobilis (Polychaeta; Nerillidae) , 2006, Journal of morphology.

[49]  G. Purschke,et al.  Evolution of body wall musculature. , 2006, Integrative and comparative biology.

[50]  E. Seaver,et al.  Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. , 2006, Developmental biology.

[51]  Joshua D. Wythe,et al.  Identification of new netrin family members in zebrafish: Developmental expression of netrin2 and netrin4 , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[52]  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.

[53]  A. Schohl,et al.  β-Catenin controls cell sorting at the notochord–somite boundary independently of cadherin-mediated adhesion , 2005, The Journal of cell biology.

[54]  A. Wanninger Immunocytochemistry of the nervous system and the musculature of the chordoid larva of Symbion pandora (Cycliophora) , 2005, Journal of morphology.

[55]  J. Gerhart,et al.  Hemichordates and the origin of chordates. , 2005, Current opinion in genetics & development.

[56]  Jun Qin,et al.  Erk Associates with and Primes GSK-3β for Its Inactivation Resulting in Upregulation of β-Catenin , 2005 .

[57]  D. Newgreen,et al.  Sox10 overexpression induces neural crest‐like cells from all dorsoventral levels of the neural tube but inhibits differentiation , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[58]  Derek L. Stemple,et al.  Structure and function of the notochord: an essential organ for chordate development , 2005, Development.

[59]  M. Sørensen Musculature in three species of Proales (Monogononta, Rotifera) stained with phalloidin-labeled fluorescent dye , 2005, Zoomorphology.

[60]  G. Purschke,et al.  Reconstruction of the musculature of Magelona cf. mirabilis (Magelonidae) and Prionospio cirrifera (Spionidae) (Polychaeta, Annelida) by phalloidin labeling and cLSM , 2005, Zoomorphology.

[61]  D. Stemple The notochord , 2004, Current Biology.

[62]  W. Sterrer,et al.  Musculature and nervous system of Gnathostomula peregrina (Gnathostomulida) shown by phalloidin labeling, immunohistochemistry, and cLSM, and their phylogenetic significance , 2004, Zoomorphology.

[63]  S. Santagata Larval development of Phoronis pallida (Phoronida): Implications for morphological convergence and divergence among larval body plans , 2004, Journal of morphology.

[64]  G. Bell,et al.  GEISHA, a whole‐mount in situ hybridization gene expression screen in chicken embryos , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[65]  R. Hochberg,et al.  The musculature of Draculiciteria tessalata (Chaetonotida, Paucitubulatina): implications for the evolution of dorsoventral muscles in Gastrotricha , 2001, Hydrobiologia.

[66]  Young-Hoon Lee,et al.  Sox9, a novel pancreatic marker in Xenopus. , 2003, The International journal of developmental biology.

[67]  G. Levi,et al.  Dlx5 regulates chondrocyte differentiation at multiple stages. , 2003, The International journal of developmental biology.

[68]  A. Schmidt‐Rhaesa,et al.  Reconstruction of the muscle system in Antygomonas sp. (Kinorhyncha, Cyclorhagida) by means of phalloidin labeling and cLSM , 2003, Journal of morphology.

[69]  A. McMahon,et al.  The Morphogen Sonic Hedgehog Is an Axonal Chemoattractant that Collaborates with Netrin-1 in Midline Axon Guidance , 2003, Cell.

[70]  V. Lefebvre,et al.  Sox5 and Sox6 are required for notochord extracellular matrix sheath formation, notochord cell survival and development of the nucleus pulposus of intervertebral discs , 2003, Development.

[71]  C. Kimmel,et al.  Shaping the zebrafish notochord , 2003, Development.

[72]  L. Holland,et al.  An amphioxus winged helix/forkhead gene, AmphiFoxD: Insights into vertebrate neural crest evolution , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[73]  L. Goodyear,et al.  Invited review: intracellular signaling in contracting skeletal muscle. , 2002, Journal of applied physiology.

[74]  Scott E Fraser,et al.  Convergent extension: the molecular control of polarized cell movement during embryonic development. , 2002, Developmental cell.

[75]  A. Meng,et al.  Zebrafish sox9b is an early neural crest marker , 2002, Development Genes and Evolution.

[76]  G. Purschke,et al.  On the absence of circular muscle elements in the body wall of Dysponetus pygmaeus (Chrysopetalidae, Polychaeta, Annelida) , 2002 .

[77]  L. Niswander,et al.  Expression of slit‐2 and slit‐3 during chick development , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[78]  S. D. Hill,et al.  Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp. I. , 2001, The Biological bulletin.

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

[80]  E. Füchtbauer,et al.  cDermo-1 expression indicates a role in avian skin development , 2001, Anatomy and Embryology.

[81]  N. Satoh,et al.  Genes expressed in the amphioxus notochord revealed by EST analysis. , 2000, Developmental biology.

[82]  P. Skoglund,et al.  Mechanisms of convergence and extension by cell intercalation. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[83]  S. Shimeld An amphioxus netrin gene is expressed in midline structures during embryonic and larval development , 2000, Development Genes and Evolution.

[84]  Y. Rao,et al.  Embryonic expression and extracellular secretion of Xenopus Slit , 2000, Neuroscience.

[85]  T. Pieler,et al.  Characterization of a subfamily of related winged helix genes, XFD-12/12′/12″ (XFLIP), during Xenopus embryogenesis , 1999, Mechanisms of Development.

[86]  M. Fürthauer,et al.  Three different noggin genes antagonize the activity of bone morphogenetic proteins in the zebrafish embryo. , 1999, Developmental biology.

[87]  J. Smith,et al.  Interference with brachyury function inhibits convergent extension, causes apoptosis, and reveals separate requirements in the FGF and activin signalling pathways. , 1999, Developmental biology.

[88]  D. Arendt,et al.  Dorsoventral axis inversion: Enteropneust anatomy links invertebrates to chordates turned upside down , 1999 .

[89]  S. Shimeld The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog , 1999, Development Genes and Evolution.

[90]  E. Davidson,et al.  A comparative molecular approach to mesodermal patterning in basal deuterostomes: the expression pattern of Brachyury in the enteropneust hemichordate Ptychodera flava. , 1999, Development.

[91]  Toshiya Yamada,et al.  Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis , 1998, Mechanisms of Development.

[92]  Ernst Hunziker,et al.  Collagen II Is Essential for the Removal of the Notochord and the Formation of Intervertebral Discs , 1998, The Journal of cell biology.

[93]  J. Rossant,et al.  Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. , 1998, Development.

[94]  C. Nüsslein-Volhard,et al.  fork head domain genes in zebrafish , 1998, Development Genes and Evolution.

[95]  A. McMahon,et al.  Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. , 1998, Genes & development.

[96]  S. Aizawa,et al.  Expression of a twist-related gene, Bbtwist, during the development of a lancelet species and its relation to cephalochordate anterior structures. , 1998, Developmental biology.

[97]  E. Robertis,et al.  The prechordal midline of the chondrocranium is defective in Goosecoid-1 mouse mutants , 1998, Mechanisms of Development.

[98]  M. Kessel,et al.  Patterning of the chick forebrain anlage by the prechordal plate. , 1997, Development.

[99]  N. Satoh,et al.  Formation of the chordamesoderm in the amphioxus embryo: Analysis with Brachyury and fork head/HNF-3 genes , 1997, Development Genes and Evolution.

[100]  Donald M. Bell,et al.  SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. , 1997, Developmental biology.

[101]  S. Shimeld Characterisation of amphioxus HNF-3 genes: conserved expression in the notochord and floor plate. , 1997, Developmental biology.

[102]  D. Arendt,et al.  Dorsal or ventral: Similarities in fate maps and gastrulation patterns in annelids, arthropods and chrodates , 1997, Mechanisms of Development.

[103]  The chordoid larva of Symbion pandora (Cycliophora) is a modified trochophore , 1996, Journal of morphology.

[104]  E. D. De Robertis,et al.  A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls. , 1996, Development.

[105]  P. Currie,et al.  Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish , 1996, Nature.

[106]  Y. Sasai,et al.  A common plan for dorsoventral patterning in Bilateria , 1996, Nature.

[107]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[108]  P. Holland,et al.  Conservation of Brachyury (T) genes in amphioxus and vertebrates: developmental and evolutionary implications. , 1995, Development.

[109]  J. Postlethwait,et al.  A homeobox gene essential for zebrafish notochord development , 1995, Nature.

[110]  E. Olson,et al.  Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. , 1995, Developmental biology.

[111]  A. McMahon,et al.  Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. , 1995, Development.

[112]  J. J. Lee,et al.  Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. , 1995, Development.

[113]  T. Jessell,et al.  Induction of motor neurons by Sonic hedgehog is independent of floor plate differentiation , 1995, Current Biology.

[114]  K. Ligon,et al.  Paraxis: a basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites. , 1995, Developmental biology.

[115]  J. Cooke,et al.  The chick Brachyury gene: developmental expression pattern and response to axial induction by localized activin. , 1995, Developmental biology.

[116]  F. Schram Animal evolution: Interrelationships of living Phyla , 1995 .

[117]  M. Jamrich,et al.  Differential expression of fork head genes during early Xenopus and zebrafish development. , 1995, Developmental genetics.

[118]  N. Patel,et al.  The novel homeodomain gene buttonless specifies differentiation and axonal guidance functions of Drosophila dorsal median cells. , 1994, Development.

[119]  D. Arendt,et al.  Inversion of dorsoventral axis? , 1994, Nature.

[120]  J. Rossant,et al.  HNF-3β is essential for node and notochord formation in mouse development , 1994, Cell.

[121]  Timothy E. Kennedy,et al.  Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord , 1994, Cell.

[122]  G. Shinn,et al.  Epithelial Origin of Mesodermal Structures in Arrowworms (Phylum Chaetognatha) , 1994 .

[123]  C. Nüsslein-Volhard,et al.  no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. , 1994, Development.

[124]  Michael E. Roberts,et al.  Ultrastructure of hatchling chaetognaths (Ferosagitta hispida): Epithelial arrangement of the mesoderm and its phylogenetic implications , 1994, Journal of morphology.

[125]  J. Rossant,et al.  HNF-3 beta is essential for node and notochord formation in mouse development. , 1994, Cell.

[126]  P. Ingham,et al.  A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos , 1993, Cell.

[127]  Andrew P. McMahon,et al.  Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity , 1993, Cell.

[128]  P. McCrea,et al.  Induction of a secondary body axis in Xenopus by antibodies to beta- catenin , 1993, The Journal of cell biology.

[129]  B. Hogan,et al.  Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. , 1993, Development.

[130]  J. Shih,et al.  Cell motility driving mediolateral intercalation in explants of Xenopus laevis. , 1992, Development.

[131]  William C. Smith,et al.  Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos , 1992, Cell.

[132]  J. Smith,et al.  Expression of a xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction , 1991, Cell.

[133]  J. Bieker,et al.  Expression of two nonallelic type II procollagen genes during Xenopus laevis embryogenesis is characterized by stage-specific production of alternatively spliced transcripts , 1991, The Journal of cell biology.

[134]  R. Keller,et al.  Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. , 1991, Development.

[135]  A. Wood,et al.  The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. , 1991, Development.

[136]  C. Kimmel,et al.  Cell movements during epiboly and gastrulation in zebrafish. , 1990, Development.

[137]  D. Wilkinson,et al.  Expression pattern of the mouse T gene and its role in mesoderm formation , 1990, Nature.

[138]  J. Gurdon,et al.  A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest , 1989, Cell.

[139]  M. Solursh,et al.  Widespread distribution of type II collagen during embryonic chick development. , 1989, Developmental biology.

[140]  R. Renkawitz-Pohl,et al.  β3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis , 1988 .

[141]  J. Shih,et al.  The function and mechanism of convergent extension during gastrulation of Xenopus laevis. , 1985, Journal of embryology and experimental morphology.

[142]  D. M. Miyamoto,et al.  Formation of the notochord in living ascidian embryos. , 1985, Journal of embryology and experimental morphology.

[143]  G. Hoyle,et al.  The Musculature of Peripatus and Its Innervation , 1980 .

[144]  D. Baskin Fine structure, functional organization and supportive role of neuroglia in Nereis. , 1971, Tissue & cell.

[145]  M. Stefanini,et al.  Fixation of Ejaculated Spermatozoa for Electron Microscopy , 1967, Nature.

[146]  E. Conklin The embryology of amphioxus , 1932 .