Evolutionary crossroads in developmental biology: Cnidaria

There is growing interest in the use of cnidarians (corals, sea anemones, jellyfish and hydroids) to investigate the evolution of key aspects of animal development, such as the formation of the third germ layer (mesoderm), the nervous system and the generation of bilaterality. The recent sequencing of the Nematostella and Hydra genomes, and the establishment of methods for manipulating gene expression, have inspired new research efforts using cnidarians. Here, we present the main features of cnidarian models and their advantages for research, and summarize key recent findings using these models that have informed our understanding of the evolution of the developmental processes underlying metazoan body plan formation.

[1]  Rafael D. Rosengarten,et al.  A Hypervariable Invertebrate Allodeterminant , 2009, Current Biology.

[2]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. , 1972, Journal of cell science.

[3]  B. Zhu,et al.  Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements , 2006, Nature.

[4]  U. Technau,et al.  Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa) , 2002, Development Genes and Evolution.

[5]  Lars Gislén,et al.  Advanced optics in a jellyfish eye , 2005, Nature.

[6]  Christoph M. Happel,et al.  WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra , 2000, Nature.

[7]  K Ikeo,et al.  Pax 6: mastering eye morphogenesis and eye evolution. , 1999, Trends in genetics : TIG.

[8]  M. Martindale,et al.  Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. , 2007, Developmental biology.

[9]  J. Lohmann,et al.  Silencing of developmental genes in Hydra. , 1999, Developmental biology.

[10]  M. Martindale,et al.  Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression. , 2007, Developmental biology.

[11]  D. Hayward,et al.  Localized expression of a dpp/BMP2/4 ortholog in a coral embryo , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  T. Bosch,et al.  Control of foot differentiation in Hydra: Phylogenetic footprinting indicates interaction of head, bud and foot patterning systems , 2005, Mechanisms of Development.

[13]  H. Bode,et al.  Continuous conversion of neuron phenotype in hydra. , 1992, Trends in genetics : TIG.

[14]  T Sugiyama,et al.  Genetic analysis of developmental mechanisms in hydra. XII. Analysis of chimaeric hydra produced from a normal and a slow-budding strain (L4). , 1984, Journal of embryology and experimental morphology.

[15]  U. Technau,et al.  Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. , 2003, Developmental biology.

[16]  T. Fujisawa,et al.  Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. , 1978, Journal of cell science.

[17]  H. le Guyader,et al.  Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). , 2008, Developmental biology.

[18]  E. Houliston,et al.  Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo , 2007, PLoS biology.

[19]  B. Galliot,et al.  Head regeneration in wild-type hydra requires de novo neurogenesis , 2007, Development.

[20]  Ronghui Xu,et al.  Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/β-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): Implications for the evolution of gastrulation , 2011, EvoDevo.

[21]  J. Finnerty,et al.  Conserved and novel gene expression between regeneration and asexual fission in Nematostella vectensis , 2009, Development Genes and Evolution.

[22]  R. Steele,et al.  Evolutionary History of the HAP2/GCS1 Gene and Sexual Reproduction in Metazoans , 2009, PloS one.

[23]  H. Bode The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. , 1996, Journal of cell science.

[24]  W. Müller,et al.  Evolution of Developmental Control Mechanisms Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras , 2010 .

[25]  D. Hayward,et al.  snail expression during embryonic development of the coral Acropora: blurring the diploblast/triploblast divide? , 2004, Development Genes and Evolution.

[26]  U. Technau,et al.  The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa) , 2002, Development Genes and Evolution.

[27]  Grigory Genikhovich,et al.  BMPs and Chordin regulate patterning of the directive axis in a sea anemone , 2009, Proceedings of the National Academy of Sciences.

[28]  H. Bode,et al.  Evolution of Developmental Control Mechanisms β-catenin plays a central role in setting up the head organizer in hydra , 2010 .

[29]  L. Salvini-Plawen On the origin and evolution of the lower Metazoa , 2009 .

[30]  Z. Kozmík,et al.  Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. , 2003, Developmental cell.

[31]  M. Martindale,et al.  An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation , 2003, Nature.

[32]  T. Fujisawa,et al.  Genetic analysis of developmental mechanisms in hydra , 2005 .

[33]  C. Hand,et al.  The Culture, Sexual and Asexual Reproduction, and Growth of the Sea Anemone Nematostella vectensis. , 1992, The Biological bulletin.

[34]  W. Müller,et al.  Ectopic head and foot formation in Hydra: diacylglycerol-induced increase in positional value and assistance of the head in foot formation. , 1990, Differentiation; research in biological diversity.

[35]  Kazuho Ikeo,et al.  Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra , 2010, Proceedings of the National Academy of Sciences.

[36]  Abraham Trembley Mémoires, pour servir à l'histoire d'un genre de polypes d'eau douce, à bras en forme de cornes , 1975 .

[37]  T. Holstein,et al.  Cell sorting during the regeneration of Hydra from reaggregated cells. , 1992, Developmental biology.

[38]  Patrick R. H. Steinmetz,et al.  A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis , 2009, Proceedings of the National Academy of Sciences.

[39]  R. de Rosa,et al.  Origins of neurogenesis, a cnidarian view. , 2009, Developmental biology.

[40]  A. Collins Phylogeny of Medusozoa and the evolution of cnidarian life cycles , 2002 .

[41]  T. Holstein,et al.  An ancient chordin-like gene in organizer formation of Hydra , 2007, Proceedings of the National Academy of Sciences.

[42]  B. Galliot,et al.  Molecular and Cellular Basis of Regeneration and Tissue Repair , 2007, Cellular and Molecular Life Sciences.

[43]  H. Bode,et al.  Head regeneration and polarity reversal inHydra attenuata can occur in the absence of DNA synthesis , 1984, Wilhelm Roux's archives of developmental biology.

[44]  C. Bamberger,et al.  The p53 Tumor Suppressor-Like Protein nvp63 Mediates Selective Germ Cell Death in the Sea Anemone Nematostella vectensis , 2007, PloS one.

[45]  M. Martindale,et al.  Molecular evidence for deep evolutionary roots of bilaterality in animal development. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[46]  David J. Miller,et al.  Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. , 2005, Trends in genetics : TIG.

[47]  J. Spring,et al.  The mesoderm specification factor twist in the life cycle of jellyfish. , 2000, Developmental biology.

[48]  The Invertebrates: Protozoa Through Ctenophora , 1940 .

[49]  T. Bosch Hydra and the evolution of stem cells , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[50]  T. Bosch,et al.  Transgenic Stem Cells in Hydra Reveal an Early Evolutionary Origin for Key Elements Controlling Self-renewal and Differentiation , 2007 .

[51]  J. Spring,et al.  Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. , 2002, Developmental biology.

[52]  P M Bode,et al.  Formation of pattern in regenerating tissue pieces of hydra attenuata. I. Head-body proportion regulation. , 1980, Developmental biology.

[53]  Dan-Eric Nilsson,et al.  The evolution of eyes and visually guided behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Cestmir Vlcek,et al.  Assembly of the cnidarian camera-type eye from vertebrate-like components , 2008, Proceedings of the National Academy of Sciences.

[55]  O. Mogensen,et al.  Effect of Voids on Angular Correlation of Positron Annihilation Photons in Molybdenum , 1972, Nature.

[56]  J. Finnerty,et al.  Regional population structure of a widely introduced estuarine invertebrate: Nematostella vectensis Stephenson in New England , 2004, Molecular ecology.

[57]  J. Smith,et al.  Evolution of Brachyury proteins: identification of a novel regulatory domain conserved within Bilateria. , 2003, Developmental biology.

[58]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. , 1974, Journal of cell science.

[59]  M. Martindale,et al.  Unexpected complexity of the Wnt gene family in a sea anemone , 2005, Nature.

[60]  M. Sheader,et al.  The anemone, Nematostella vectensis, in Britain: considerations for conservation management , 1997 .

[61]  T. Bosch,et al.  More than just orphans: are taxonomically-restricted genes important in evolution? , 2009, Trends in genetics : TIG.

[62]  W. Gehring,et al.  Flexibly deployed Pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish , 2010, Proceedings of the National Academy of Sciences.

[63]  T. Holstein,et al.  Phenotypic maturation of neurons and continuous precursor migration in the formation of the peduncle nerve net in Hydra. , 1996, Developmental biology.

[64]  H. Watanabe,et al.  The Wnt code: cnidarians signal the way , 2006, Oncogene.

[65]  E. Ball,et al.  Cnidarians and ancestral genetic complexity in the animal kingdom. , 2005, Trends in genetics : TIG.

[66]  T. Holstein The morphogenesis of nematocytes in Hydra and Forskålia: an ultrastructural study. , 1981, Journal of ultrastructure research.

[67]  Grigory Genikhovich,et al.  The starlet sea anemone Nematostella vectensis: an anthozoan model organism for studies in comparative genomics and functional evolutionary developmental biology. , 2009, Cold Spring Harbor protocols.

[68]  J. Finnerty,et al.  Investigating the origins of triploblasty: `mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa) , 2004, Development.

[69]  Romain Derelle,et al.  A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica , 2008, Development.

[70]  J. Finnerty,et al.  Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone , 2004, Science.

[71]  R. D. Campbell Elimination by Hydra interstitial and nerve cells by means of colchicine. , 1976, Journal of cell science.

[72]  M. Miller,et al.  Oocyte development in Hydra involves selection from competent precursor cells. , 2000, Developmental biology.

[73]  J. Finnerty,et al.  Rising starlet: the starlet sea anemone, Nematostella vectensis. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[74]  U. Technau,et al.  Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. , 2004, Developmental biology.

[75]  D. Hayward,et al.  Coral development: from classical embryology to molecular control. , 2002, The International journal of developmental biology.

[76]  Nicholas H. Putnam,et al.  Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization , 2007, Science.

[77]  R. Saint,et al.  EST Analysis of the Cnidarian Acropora millepora Reveals Extensive Gene Loss and Rapid Sequence Divergence in the Model Invertebrates , 2003, Current Biology.

[78]  David Q. Matus,et al.  A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. , 2006, Seminars in cell & developmental biology.

[79]  Grigory Genikhovich,et al.  The blastoporal organiser of a sea anemone , 2007, Current Biology.

[80]  David J. Duffy,et al.  Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration , 2010, Development.

[81]  A. Böttger,et al.  The Notch signaling pathway in the cnidarian Hydra. , 2007, Developmental biology.

[82]  J. Lohmann,et al.  Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[83]  Benjamin M. Wheeler,et al.  The dynamic genome of Hydra , 2010, Nature.

[84]  P. Tardent,et al.  Migration of I-cells from ectoderm to endoderm in Hydra attenuata Pall (Cnidaria, Hydrozoa) and their subsequent differentiation. , 1984, Developmental biology.

[85]  H. Bode,et al.  HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. , 2000, Development.

[86]  B. Schierwater,et al.  Axial Patterning and Diversification in the Cnidaria Predate the Hox System , 2006, Current Biology.

[87]  W. Gehring,et al.  Evolution and Functional Diversity of Jellyfish Opsins , 2008, Current Biology.

[88]  M. Manuel,et al.  Clytia hemisphaerica: a jellyfish cousin joins the laboratory. , 2010, Trends in genetics : TIG.

[89]  D. Green,et al.  Knockdown of Actin and Caspase Gene Expression by RNA Interference in the Symbiotic Anemone Aiptasia pallida , 2007, The Biological Bulletin.

[90]  Ethel Nicholson Browne,et al.  The production of new hydranths in Hydra by the insertion of small grafts , 1909 .

[91]  R. D. Campbell,et al.  Phylogeny and biogeography of Hydra (Cnidaria: Hydridae) using mitochondrial and nuclear DNA sequences. , 2010, Molecular phylogenetics and evolution.

[92]  D. Hayward,et al.  New tricks with old genes: the genetic bases of novel cnidarian traits. , 2010, Trends in genetics : TIG.

[93]  A. Böttger,et al.  Genetic screen for signal peptides in Hydra reveals novel secreted proteins and evidence for non-classical protein secretion. , 2006, European journal of cell biology.

[94]  U. Technau,et al.  Origin and evolution of endoderm and mesoderm. , 2003, The International journal of developmental biology.

[95]  B. Galliot,et al.  Origin of anterior patterning. How old is our head? , 2000, Trends in genetics : TIG.

[96]  Morgane Thomas-Chollier,et al.  A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution , 2010, BMC Evolutionary Biology.

[97]  Bert Hobmayer,et al.  Wnt/β-Catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra , 2009, Proceedings of the National Academy of Sciences.

[98]  A. Gierer,et al.  Regeneration of hydra from reaggregated cells. , 1972, Nature: New biology.

[99]  H. Bode,et al.  Formation of the head organizer in hydra involves the canonical Wnt pathway , 2005, Development.

[100]  H. Macwilliams Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. , 1983, Developmental biology.

[101]  P. Wincker,et al.  Are Hox Genes Ancestrally Involved in Axial Patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria) , 2009, PloS one.

[102]  T. Holstein,et al.  Cnidarians: An evolutionarily conserved model system for regeneration? , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[103]  U. Frank,et al.  Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. , 2006, Developmental biology.

[104]  H. Bode,et al.  Interstitial cell migration in Hydra attenuata. I. Quantitative description of cell movements. , 1984, Developmental biology.

[105]  T. Bosch,et al.  A Novel Gene Family Controls Species-Specific Morphological Traits in Hydra , 2008, PLoS biology.

[106]  A. Böttger,et al.  GFP expression in Hydra: lessons from the particle gun , 2002, Development Genes and Evolution.

[107]  H. Bode,et al.  Characterization of the head organizer in hydra. , 2002, Development.

[108]  C. N. David,et al.  Characterization of interstitial stem cells in hydra by cloning. , 1977, Developmental biology.

[109]  Grigory Genikhovich,et al.  Early development and axis specification in the sea anemone Nematostella vectensis. , 2007, Developmental biology.

[110]  U. Technau,et al.  Characterization of myostatin/gdf8/11 in the starlet sea anemone Nematostella vectensis. , 2009, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[111]  H. Bode,et al.  Parameters of self-organization in Hydra aggregates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[112]  D. Hayward,et al.  A simple plan — cnidarians and the origins of developmental mechanisms , 2004, Nature Reviews Genetics.

[113]  T. Holstein,et al.  Morphology and morphodynamics of the stenotele nematocyst of Hydra attenuata Pall. (Hydrozoa, Cnidaria) , 2004, Cell and Tissue Research.

[114]  A. Bieller,et al.  Stepwise transfer from high to low lithium concentrations increases the head-forming potential in Hydra vulgaris and possibly activates the PI cycle. , 1996, Developmental biology.

[115]  H. Macwilliams Hydra transplantation phenomena and the mechanism of Hydra head regeneration: II. Properties of the head activation , 1983 .

[116]  C. David,et al.  A genomic view of 500 million years of cnidarian evolution. , 2011, Trends in genetics : TIG.

[117]  M. Sheader,et al.  The genetic structure of the rare lagoonal sea anemone, Nematostella vectensis Stephenson (Cnidaria; Anthozoa) in the United Kingdom based on RAPD analysis , 2002, Molecular ecology.

[118]  David J. Miller,et al.  Cryptic complexity captured: the Nematostella genome reveals its secrets. , 2008, Trends in genetics : TIG.

[119]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[120]  C. Weaver,et al.  Move it or lose it: axis specification in Xenopus , 2004, Development.

[121]  V. Schmid,et al.  Animal pole determinants define oral-aboral axis polarity and endodermal cell-fate in hydrozoan jellyfish Podocoryne carnea. , 2006, Developmental biology.

[122]  M. Kroiher,et al.  Cell proliferation and early differentiation during embryonic development and metamorphosis of Hydractinia echinata. , 1988, Development.

[123]  H. Bode,et al.  Embryogenesis in hydra. , 1997, The Biological bulletin.

[124]  A. Gierer,et al.  Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. , 1974, Journal of cell science.

[125]  M. Martindale,et al.  Dorso/Ventral Genes Are Asymmetrically Expressed and Involved in Germ-Layer Demarcation during Cnidarian Gastrulation , 2006, Current Biology.

[126]  T. Holstein,et al.  Pattern of epithelial cell cycling in hydra. , 1991, Developmental biology.

[127]  B. Schierwater,et al.  Solution to the phylogenetic enigma of Tetraplatia, a worm-shaped cnidarian , 2006, Biology Letters.

[128]  H. Bode,et al.  Formation of pattern in regenerating tissue pieces of Hydra attenuata. II. Degree of proportion regulation is less in the hypostome and tentacle zone than in the tentacles and basal disc. , 1984, Developmental biology.

[129]  H. Bode,et al.  Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction , 2007, Development.

[130]  T. Holstein,et al.  Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. , 2006, Developmental biology.

[131]  S. Sunagawa,et al.  Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont , 2009, BMC Genomics.

[132]  J. Martinou,et al.  Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. , 2009, Developmental cell.

[133]  A. Collins,et al.  Exceptionally Preserved Jellyfishes from the Middle Cambrian , 2007, PloS one.

[134]  H. Bode,et al.  HyBra1, a Brachyury homologue, acts during head formation in Hydra. , 1999, Development.

[135]  F. Rentzsch,et al.  FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis , 2008, Development.

[136]  B. Galliot Conserved and divergent genes in apex and axis development of cnidarians. , 2000, Current opinion in genetics & development.

[137]  Oleg Simakov,et al.  Multiple Wnts are involved in Hydra organizer formation and regeneration. , 2009, Developmental biology.

[138]  B. Galliot,et al.  Regeneration and tissue repair: themes and variations. , 2008, Cellular and molecular life sciences : CMLS.

[139]  Anders Garm,et al.  Structure and optics of the eyes of the box jellyfish Chiropsella bronzie , 2009, Journal of Comparative Physiology A.