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Cnidaria

  • Chapter
Evolutionary Developmental Biology of Invertebrates 1

Abstract

Cnidaria is a large animal phylum comprising mostly marine, with few species that have adapted to freshwater environments. Molecular phylogenies place the Cnidaria as a sister group to the Bilateria. The sister group relationship between Cnidaria and Bilateria is very robust and puts this phylum in a strategic position for the understanding of the evolution of key bilaterian features, such as the third germ layer (the mesoderm), the central nervous system, and bilaterality. We will give a short historical account and then highlight recent advances in the field of evolution and development from a variety of cnidarian model systems.

Chapter vignette artwork by Brigitte Baldrian. © Brigitte Baldrian and Andreas Wanninger.

Although recognized as a subtaxon of Cnidaria by most recent phylogenetic analyses, the Myxozoa are covered separately in the following chapter of this volume.

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References

  • Ambrosone A, Marchesano V, Tino A, Hobmayer B, Tortiglione C (2012) Hymyc1 downregulation promotes stem cell proliferation in Hydra vulgaris. PLoS One 7(1):e30660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Augustin R, Franke A, Khalturin K, Kiko R, Siebert S, Hemmrich G, Bosch TC (2006) Dickkopf related genes are components of the positional value gradient in Hydra. Dev Biol 296(1):62–70

    CAS  PubMed  Google Scholar 

  • Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, Saint R, Harrison PL, Miller DJ (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46(4):671–678

    CAS  PubMed  Google Scholar 

  • Bielen H, Oberleitner S, Marcellini S, Gee L, Lemaire P, Bode HR, Rupp R, Technau U (2007) Divergent functions of two ancient Hydra brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction. Development 134(23):4187–4197

    CAS  PubMed  Google Scholar 

  • Bode HR (1992) Continuous conversion of neuron phenotype in Hydra. Trends Genet 8(8):279–284

    CAS  PubMed  Google Scholar 

  • Bode PM, Bode HR (1980) Formation of pattern in regenerating tissue pieces of Hydra attenuata. I. Head-body proportion regulation. Dev Biol 78(2):484–496

    CAS  PubMed  Google Scholar 

  • Bode HR, Heimfeld S, Chow MA, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122(2):577–585

    CAS  PubMed  Google Scholar 

  • Bode PM, Awad TA, Koizumi O, Nakashima Y, Grimmelikhuijzen CJ, Bode HR (1988) Development of the two-part pattern during regeneration of the head in Hydra. Development 102(1):223–235

    CAS  PubMed  Google Scholar 

  • Boehm AM, Khalturin K, Anton-Erxleben F, Hemmrich G, Klostermeier UC, Lopez-Quintero JA, Oberg HH, Puchert M, Rosenstiel P, Wittlieb J, Bosch TC (2012) FoxO is a critical regulator of stem cell maintenance in immortal Hydra. Proc Natl Acad Sci U S A 109(48):19697–19702

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boelsterli U (1977) An electron microscopic study of early developmental stages, myogenesis, oogenesis, and cnidogenesis in the anthomedusa, Podocoryne carnea M. Sars. J Morphol 154:259–289

    CAS  PubMed  Google Scholar 

  • Bosch TC (2012a) Understanding complex host-microbe interactions in Hydra. Gut Microbes 3(4):345–351

    PubMed Central  PubMed  Google Scholar 

  • Bosch TC (2012b) What Hydra has to say about the role and origin of symbiotic interactions. Biol Bull 223(1):78–84

    PubMed  Google Scholar 

  • Broun M, Bode HR (2002) Characterization of the head organizer in Hydra. Development 129(4):875–884

    CAS  PubMed  Google Scholar 

  • Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in Hydra involves the canonical Wnt pathway. Development 132(12):2907–2916

    CAS  PubMed  Google Scholar 

  • Browne E (1909) The production of new Hydrants by the insertion of small grafts. J Exp Zool 7:1–37

    Google Scholar 

  • Byrum CA, Martindale MQ (2004) Gastrulation in the Cnidaria and Ctenophora. In: Stern CD (ed) Gastrulation. From cells to embryos. Cold Spring Harbor Laboratory Press, New York, pp 33–50

    Google Scholar 

  • Campbell RD (1976) Elimination by Hydra interstitial and nerve cells by means of colchicine. J Cell Sci 21(1):1–13

    CAS  PubMed  Google Scholar 

  • Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PR, Zhang X, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Bottger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TC, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464(7288):592–596

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W, Martinou JC, Galliot B (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive Hydra head regeneration. Dev Cell 17(2):279–289

    CAS  PubMed  Google Scholar 

  • Chourrout D, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, de Jong P, Steele RE, Technau U (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442(7103):684–687

    CAS  PubMed  Google Scholar 

  • Collins, AG (2002) Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J Evol Biol 15: 418–432

    Google Scholar 

  • Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B (2006) Medusozoan Phylogeny and Character Evolution Clarified by New Large and Small Subunit rDNA Data and an Assessment of the Utility of Phylogenetic Mixture Models. Syst Biol 55(1):97–115

    Google Scholar 

  • Darling JA, Reitzel AM, Finnerty JR (2004) Regional population structure of a widely introduced estuarine invertebrate: nematostella vectensis Stephenson in New England. Mol Ecol 13(10):2969–2981

    Google Scholar 

  • Darling JA, Reitzel AR, Burton PM, Mazza ME, Ryan JF, Sullivan JC, Finnerty JR (2005) Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 27(2):211–221

    CAS  PubMed  Google Scholar 

  • David CN (1973) A quantitative method for maceration of Hydra tissue. Wilhelm Roux Arch 171:259–268

    Google Scholar 

  • David CN (2012) Interstitial stem cells in Hydra: multipotency and decision-making. Int J Dev Biol 56(6–8):489–497

    PubMed  Google Scholar 

  • David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11(2):557–568

    CAS  PubMed  Google Scholar 

  • David CN, MacWilliams H (1978) Regulation of the self-renewal probability in Hydra stem cell clones. Proc Natl Acad Sci U S A 75(2):886–890

    CAS  PubMed Central  PubMed  Google Scholar 

  • David CN, Murphy S (1977) Characterization of interstitial stem cells in Hydra by cloning. Dev Biol 58(2):372–383

    CAS  PubMed  Google Scholar 

  • David CN, Plotnick I (1980) Distribution of interstitial stem cells in Hydra. Dev Biol 76(1):175–184

    CAS  PubMed  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76(2):229–261

    CAS  PubMed Central  PubMed  Google Scholar 

  • DuBuc TQ, Ryan JF, Shinzato C, Satoh N, Martindale MQ (2012) Coral comparative genomics reveal expanded Hox cluster in the cnidarian-bilaterian ancestor. Integr Comp Biol 52(6):835–841

    CAS  PubMed  Google Scholar 

  • Duffy DJ, Plickert G, Kuenzel T, Tilmann W, Frank U (2010) Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration. Development 137(18):3057–3066

    CAS  PubMed  Google Scholar 

  • Elms P, Siggers P, Napper D, Greenfield A, Arkell R (2003) Zic2 is required for neural crest formation and hindbrain patterning during mouse development. Dev Biol 264(2):391–406

    CAS  PubMed  Google Scholar 

  • Engel U, Ozbek S, Streitwolf-Engel R, Petri B, Lottspeich F, Holstein TW (2002) Nowa, a novel protein with minicollagen Cys-rich domains, is involved in nematocyst formation in Hydra. J Cell Sci 115(Pt 20):3923–3934

    CAS  PubMed  Google Scholar 

  • Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: hox and dpp expression in a sea anemone. Science 304(5675):1335–1337

    Google Scholar 

  • Frank U, Leitz T, Muller WA (2001) The hydroid Hydractinia: a versatile, informative cnidarian representative. Bioessays 23(10):963–971

    CAS  PubMed  Google Scholar 

  • Franzenburg S, Fraune S, Kunzel S, Baines JF, Domazet-Loso T, Bosch TC (2012) MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. Proc Natl Acad Sci U S A 109(47):19374–19379

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franzenburg S, Walter J, Kunzel S, Wang J, Baines JF, Bosch TC, Fraune S (2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci U S A 110(39):E3730–E3738

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fraune S, Bosch TC (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci U S A 104(32):13146–13151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freeman G (1981a) The cleavage initiation site establishes the posterior pole of the hydrozoan embryo. Roux’s Arch Dev Biol 190:123–125

    Google Scholar 

  • Freeman G (1981b) The role of polarity in the development of the hydrozoan planula larva. Roux’s Arch Dev Biol 190:168–184

    Google Scholar 

  • Freeman G, Miller RL (1982) Hydrozoan eggs can only be fertilized at the site of the polar body formation. Dev Biol 94:142–152

    CAS  PubMed  Google Scholar 

  • Fritzenwanker JH, Technau U (2002) Induction of gametogenesis in the basal cnidarian Nematostella vectensis(Anthozoa). Dev Genes Evol 212(2):99–103

    PubMed  Google Scholar 

  • Fritzenwanker JH, Saina M, Technau U (2004) Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275(2):389–402

    CAS  PubMed  Google Scholar 

  • Fritzenwanker JH, Genikhovich G, Kraus Y, Technau U (2007) Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol 310(2):264–279

    CAS  PubMed  Google Scholar 

  • Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst EM, Dirksen P, Bohm AM, Hemmrich G, Sommer F, Domazet-Loso T, Klostermeier UC, Anton-Erxleben F, Rosenstiel P, Bosch TC, Khalturin K (2014) Regulation of polyp-to-jellyfish transition in Aurelia aurita. Curr Biol 24(3):263–273

    CAS  PubMed  Google Scholar 

  • Galliot B, Quiquand M (2011) A two-step process in the emergence of neurogenesis. Eur J Neurosci 34(6):847–862

    PubMed  Google Scholar 

  • Galliot B, Quiquand M, Ghila L, de Rosa R, Miljkovic-Licina M, Chera S (2009) Origins of neurogenesis, a cnidarian view. Dev Biol 332(1):2–24

    CAS  PubMed  Google Scholar 

  • Garm A, Coates MM, Gad R, Seymour J, Nilsson DE (2007a) The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193(5):547–557

    CAS  PubMed  Google Scholar 

  • Garm A, O’Connor M, Parkefelt L, Nilsson DE (2007b) Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol 210(Pt 20):3616–3623

    CAS  PubMed  Google Scholar 

  • Garm A, Andersson F, Nilsson DE (2008) Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. Vision Res 48(8):1061–1073

    CAS  PubMed  Google Scholar 

  • Garm A, Oskarsson M, Nilsson DE (2011) Box jellyfish use terrestrial visual cues for navigation. Curr Biol 21(9):798–803

    CAS  PubMed  Google Scholar 

  • Garm A, Bielecki J, Petie R, Nilsson DE (2012) Opposite patterns of diurnal activity in the box jellyfish Tripedalia cystophora and Copula sivickisi. Biol Bull 222(1):35–45

    CAS  PubMed  Google Scholar 

  • Gauchat D, Kreger S, Holstein T, Galliot B (1998) prdl-a, a gene marker for Hydra apical differentiation related to triploblastic paired-like head-specific genes. Development 125(9):1637–1645

    CAS  PubMed  Google Scholar 

  • Gauchat D, Escriva H, Miljkovic-Licina M, Chera S, Langlois MC, Begue A, Laudet V, Galliot B (2004) The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev Biol 275(1):104–123

    CAS  PubMed  Google Scholar 

  • Gee L, Hartig J, Law L, Wittlieb J, Khalturin K, Bosch TC, Bode HR (2010) beta-catenin plays a central role in setting up the head organizer in Hydra. Dev Biol 340(1):116–124

    CAS  PubMed  Google Scholar 

  • Gehring WJ, Kloter U, Suga H (2009) Evolution of the Hox gene complex from an evolutionary ground state. Curr Top Dev Biol 88:35–61

    CAS  PubMed  Google Scholar 

  • Genikhovich G, Technau U (2009a) In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps. CSH Protoc 2009(9):pdb prot5282

    Google Scholar 

  • Genikhovich G, Technau U (2009b) The starlet sea anemone Nematostella vectensis: an anthozoan model organism for studies in comparative genomics and functional evolutionary developmental biology. CSH Protoc 2009(9):pdb emo129

    Google Scholar 

  • Genikhovich G, Technau U (2011) Complex functions of Mef2 splice variants in the differentiation of endoderm and of a neuronal cell type in a sea anemone. Development 138(22):4911–4919

    CAS  PubMed  Google Scholar 

  • Genikhovich G, Fried P, Prünster MM, Schinko JB, Gilles AF, Fredman D, Meier K, Iber D, Technau U (2015) Axis patterning by BMPs: cnidarian network reveals evolutionary constraints. Cell Rep pii: S2211–1247(15)00181–00183

    Google Scholar 

  • Genikhovich G, Kurn U, Hemmrich G, Bosch TC (2006) Discovery of genes expressed in Hydra embryogenesis. Dev Biol 289(2):466–481

    CAS  PubMed  Google Scholar 

  • Gierer A, Meinhardt H (1972) A theory of biological pattern formation. Kybernetik 12(1):30–39

    CAS  PubMed  Google Scholar 

  • Gierer A, Berking S, Bode H, David CN, Flick K, Hansmann G, Schaller H, Trenkner E (1972) Regeneration of Hydra from reaggregated cells. Nat New Biol 239(91):98–101

    CAS  PubMed  Google Scholar 

  • Grasso LC, Negri AP, Foret S, Saint R, Hayward DC, Miller DJ, Ball EE (2011) The biology of coral metamorphosis: molecular responses of larvae to inducers of settlement and metamorphosis. Dev Biol 353(2):411–419

    CAS  PubMed  Google Scholar 

  • Graziussi DF, Suga H, Schmid V, Gehring WJ (2012) The “eyes absent” (eya) gene in the eye-bearing hydrozoan jellyfish Cladonema radiatum: conservation of the retinal determination network. J Exp Zool B Mol Dev Evol 318(4):257–267

    CAS  PubMed  Google Scholar 

  • Grens A, Mason E, Marsh JL, Bode HR (1995) Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. Development 121(12):4027–4035

    CAS  PubMed  Google Scholar 

  • Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW (2006a) The Wnt code: cnidarians signal the way. Oncogene 25(57):7450–7460

    CAS  PubMed  Google Scholar 

  • Guder C, Pinho S, Nacak TG, Schmidt HA, Hobmayer B, Niehrs C, Holstein TW (2006b) An ancient Wnt-Dickkopf antagonism in Hydra. Development 133(5):901–911

    CAS  PubMed  Google Scholar 

  • Gur Barzilai M, Reitzel AM, Kraus JE, Gordon D, Technau U, Gurevitz M, Moran Y (2012) Convergent evolution of sodium ion selectivity in metazoan neuronal signaling. Cell Rep 2(2):242–248

    PubMed Central  PubMed  Google Scholar 

  • Hager G, David CN (1997) Pattern of differentiated nerve cells in Hydra is determined by precursor migration. Development 124(2):569–576

    CAS  PubMed  Google Scholar 

  • Hanaoka K (1934) Notes to the early development of a stalked medusa. Proc Imp Acad Jpn 10:117–120

    Google Scholar 

  • Hand C, Uhlinger KR (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 182:169–176

    Google Scholar 

  • Hartl M, Mitterstiller AM, Valovka T, Breuker K, Hobmayer B, Bister K (2010) Stem cell-specific activation of an ancestral myc protooncogene with conserved basic functions in the early metazoan Hydra. Proc Natl Acad Sci U S A 107(9):4051–4056

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hassel M, Bieller A (1996) Stepwise transfer from high to low lithium concentrations increases the head-forming potential in Hydra vulgaris and possibly activates the PI cycle. Dev Biol 177(2):439–448

    CAS  PubMed  Google Scholar 

  • Hassel M, Albert K, Hofheinz S (1993) Pattern formation in Hydra vulgaris is controlled by lithium-sensitive processes. Dev Biol 156(2):362–371

    CAS  PubMed  Google Scholar 

  • Hayakawa E, Fujisawa C, Fujisawa T (2004) Involvement of Hydra achaete-scute gene CnASH in the differentiation pathway of sensory neurons in the tentacles. Dev Genes Evol 214(10):486–492

    CAS  PubMed  Google Scholar 

  • Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci U S A 99(12):8106–8111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hayward DC, Hetherington S, Behm CA, Grasso LC, Forêt S, Miller DJ, Ball EE (2011) Differential gene expression at coral settlement and metamorphosis – a subtractive hybridization study. PLoS One 6(10):e26411

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hemmrich G, Anokhin B, Zacharias H, Bosch TC (2007) Molecular phylogenetics in Hydra, a classical model in evolutionary developmental biology. Mol Phylogenet Evol 44(1):281–290

    CAS  PubMed  Google Scholar 

  • Hemmrich G, Khalturin K, Boehm AM, Puchert M, Anton-Erxleben F, Wittlieb J, Klostermeier UC, Rosenstiel P, Oberg HH, Domazet-Loso T, Sugimoto T, Niwa H, Bosch TC (2012) Molecular signatures of the three stem cell lineages in Hydra and the emergence of stem cell function at the base of multicellularity. Mol Biol Evol 29(11):3267–3280

    CAS  PubMed  Google Scholar 

  • Hobmayer E, Holstein TW, David CN (1990) Tentacle morphogenesis in Hydra. II. Formation of a complex between a sensory nerve cell and a battery cell. Development 109:897–904

    Google Scholar 

  • Hobmayer B, Holstein TW, David CN (1997) Stimulation of tentacle and bud formation by the neuropeptide head activator in Hydra magnipapillata. Dev Biol 183(1):1–8

    CAS  PubMed  Google Scholar 

  • Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbacher U, Holstein TW (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407(6801):186–189

    CAS  PubMed  Google Scholar 

  • Holstein TW (2008) Wnt signaling in cnidarians. Methods Mol Biol 469:47–54

    CAS  PubMed  Google Scholar 

  • Holstein TW (2012) The evolution of the Wnt pathway. Cold Spring Harb Perspect Biol 4(7):a007922

    PubMed Central  PubMed  Google Scholar 

  • Holstein T, Tardent P (1984) An ultrahigh-speed analysis of exocytosis: nematocyst discharge. Science 223(4638):830–833

    CAS  PubMed  Google Scholar 

  • Holstein TW, Hobmayer E, David CN (1991) Pattern of epithelial cell cycling in Hydra. Dev Biol 148(2):602–611

    CAS  PubMed  Google Scholar 

  • Holstein TW, Benoit M, Herder GV, David CN, Wanner G, Gaub HE (1994) Fibrous mini-collagens in Hydra nematocysts. Science 265(5170):402–404

    CAS  PubMed  Google Scholar 

  • Holstein TW, Hobmayer E, Technau U (2003) Cnidarians: an evolutionarily conserved model system for regeneration? Dev Dyn 226(2):257–267

    CAS  PubMed  Google Scholar 

  • Houliston E, Momose T, Manuel M (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 26(4):159–167

    CAS  PubMed  Google Scholar 

  • Hudry B, Thomas-Chollier M, Volovik Y, Duffraisse M, Dard A, Frank D, Technau U, Merabet S (2014) Molecular insights into the origin of the Hox-TALE patterning system. eLife 3:e01939

    PubMed Central  PubMed  Google Scholar 

  • Hwang JS, Takaku Y, Momose T, Adamczyk P, Ozbek S, Ikeo K, Khalturin K, Hemmrich G, Bosch TC, Holstein TW, David CN, Gojobori T (2010) Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra. Proc Natl Acad Sci U S A 107(43):18539–18544

    CAS  PubMed Central  PubMed  Google Scholar 

  • Juliano CE, Reich A, Liu N, Gotzfried J, Zhong M, Uman S, Reenan RA, Wessel GM, Steele RE, Lin H (2014) PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells. Proc Natl Acad Sci U S A 111(1):337–342

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV (2013) Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol Biol 13:5

    PubMed Central  PubMed  Google Scholar 

  • Khalturin K, Anton-Erxleben F, Milde S, Plotz C, Wittlieb J, Hemmrich G, Bosch TC (2007) Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev Biol 309(1):32–44

    CAS  PubMed  Google Scholar 

  • Koch AW, Holstein TW, Mala C, Kurz E, Engel J, David CN (1998) Spinalin, a new glycine- and histidine-rich protein in spines of Hydra nematocysts. J Cell Sci 111(Pt 11):1545–1554

    CAS  PubMed  Google Scholar 

  • Koizumi O, Bode HR (1991) Plasticity in the nervous system of adult Hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J Neurosci 11(7):2011–2020

    CAS  PubMed  Google Scholar 

  • Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13(24):2190–2195

    CAS  PubMed  Google Scholar 

  • Kowalewsky A (1884) Zur Entwicklung der Lucernaria (vorläufige Mittelung). Zool Anz 7:712–717

    Google Scholar 

  • Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5(5):773–785

    CAS  PubMed  Google Scholar 

  • Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, Strnad H, Kawamura S, Piatigorsky J, Paces V, Vlcek C (2008) Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci U S A 105(26):8989–8993

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kraus Y, Technau U (2006) Gastrulation in the sea anemone Nematostella vectensis occurs by invagination and immigration: an ultrastructural study. Dev Genes Evol 216(3):119–132

    PubMed  Google Scholar 

  • Kraus Y, Fritzenwanker JH, Genikhovich G, Technau U (2007) The blastoporal organiser of a sea anemone. Curr Biol 17(20):R874–R876

    CAS  PubMed  Google Scholar 

  • Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc Biol Sci 280(1755):20122328

    PubMed Central  PubMed  Google Scholar 

  • Kumburegama S, Wijesena N, Xu R, Wikramanayake AH (2011) Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/beta-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): implications for the evolution of gastrulation. EvoDevo 2(1):2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuniyoshi H, Okumura I, Kuroda R, Tsujita N, Arakawa K, Shoji J, Saito T, Osada H (2012) Indomethacin induction of metamorphosis from the asexual stage to sexual stage in the moon jellyfish, Aurelia aurita. Biosci Biotechnol Biochem 76(7):1397–1400

    CAS  PubMed  Google Scholar 

  • Kunzel T, Heiermann R, Frank U, Muller W, Tilmann W, Bause M, Nonn A, Helling M, Schwarz RS, Plickert G (2010) Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras. Dev Biol 348(1):120–129

    PubMed  Google Scholar 

  • Kurz EM, Holstein TW, Petri BM, Engel J, David CN (1991) Mini-collagens in Hydra nematocytes. J Cell Biol 115(4):1159–1169

    CAS  PubMed  Google Scholar 

  • Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433(7022):156–160

    CAS  PubMed  Google Scholar 

  • Layden MJ, Martindale, MQ (2014) Non-canonical Notch signaling represents an ancestral mechanism to regulate neural differentiation. Evodevo 5:30

    Google Scholar 

  • Layden MJ, Boekhout M, Martindale MQ (2012) Nematostella vectensis achaete-scute homolog NvashA regulates embryonic ectodermal neurogenesis and represents an ancient component of the metazoan neural specification pathway. Development 139(5):1013–1022

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee PN, Pang K, Matus DQ, Martindale MQ (2006) A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17(2):157–167

    PubMed  Google Scholar 

  • Lee PN, Kumburegama S, Marlow HQ, Martindale MQ, Wikramanayake AH (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol 310(1):169–186

    CAS  PubMed  Google Scholar 

  • Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330(1):186–199

    CAS  PubMed  Google Scholar 

  • Lindgens D, Holstein TW, Technau U (2004) Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. Development 131(1):191–201

    CAS  PubMed  Google Scholar 

  • Littlefield CL, Bode HR (1986) Germ cells in Hydra oligactis males. II. Evidence for a subpopulation of interstitial stem cells whose differentiation is limited to sperm production. Dev Biol 116(2):381–386

    CAS  PubMed  Google Scholar 

  • Littlefield CL, Dunne JF, Bode HR (1985) Spermatogenesis in Hydra oligactis. I. Morphological description and characterization using a monoclonal antibody specific for cells of the spermatogenic pathway. Dev Biol 110(2):308–320

    CAS  PubMed  Google Scholar 

  • Littlefield CL, Finkemeier C, Bode HR (1991) Spermatogenesis in Hydra oligactis. II. How temperature controls the reciprocity of sexual and asexual reproduction. Dev Biol 146(2):292–300

    CAS  PubMed  Google Scholar 

  • MacWilliams HK (1982) Numerical simulations of Hydra head regeneration using a proportion-regulating version of the Gierer-Meinhardt model. J Theor Biol 99(4):681–703

    CAS  PubMed  Google Scholar 

  • MacWilliams HK (1983a) Hydra transplantation phenomena and the mechanism of Hydra head regeneration. I. Properties of the head inhibition. Dev Biol 96(1):217–238

    CAS  PubMed  Google Scholar 

  • MacWilliams HK (1983b) Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. Dev Biol 96(1):239–257

    CAS  PubMed  Google Scholar 

  • Magie CR, Pang K, Martindale MQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215(12):618–630

    CAS  PubMed  Google Scholar 

  • Magie CR, Daly M, Martindale MQ (2007) Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression. Dev Biol 305(2):483–497

    CAS  PubMed  Google Scholar 

  • Mahoney JL, Graugnard EM, Mire P, Watson GM (2011) Evidence for involvement of TRPA1 in the detection of vibrations by hair bundle mechanoreceptors in sea anemones. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197(7):729–742

    CAS  PubMed  Google Scholar 

  • Marcum BA, Campbell RD (1978) Development of Hydra lacking nerve and interstitial cells. J Cell Sci 29:17–33

    CAS  PubMed  Google Scholar 

  • Marlow HQ, Srivastava M, Matus DQ, Rokhsar D, Martindale MQ (2009) Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol 69(4):235–254

    CAS  PubMed  Google Scholar 

  • Marlow H, Roettinger E, Boekhout M, Martindale MQ (2012) Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev Biol 362(2):295–308

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marlow H, Matus DQ, Martindale MQ (2013) Ectopic activation of the canonical wnt signaling pathway affects ectodermal patterning along the primary axis during larval development in the anthozoan Nematostella vectensis. Dev Biol 380(2):324–334

    CAS  PubMed  Google Scholar 

  • Martin VJ, Littlefield CL, Archer WE, Bode HR (1997) Embryogenesis in Hydra. Biol Bull 192(3):345–363

    CAS  PubMed  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: “mesodermal” gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131(10):2463–2474

    CAS  PubMed  Google Scholar 

  • Marques AC, Collins AG (2004) Cladistic analysis of Medusozoa and cnidarian evolution. Invert Biol 123: 23–42

    Google Scholar 

  • Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, Martindale MQ (2006a) Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci U S A 103(30):11195–11200

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matus DQ, Thomsen GH, Martindale MQ (2006b) Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr Biol 16(5):499–505

    CAS  PubMed  Google Scholar 

  • Matus DQ, Pang K, Daly M, Martindale MQ (2007) Expression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis. Evol Dev 9(1):25–38

    CAS  PubMed  Google Scholar 

  • Meinhardt H (1993) A model for pattern formation of hypostome, tentacles, and foot in Hydra: how to form structures close to each other, how to form them at a distance. Dev Biol 157(2):321–333

    CAS  PubMed  Google Scholar 

  • Meinhardt H (2012) Modeling pattern formation in Hydra: a route to understanding essential steps in development. Int J Dev Biol 56(6–8):447–462

    CAS  PubMed  Google Scholar 

  • Meinhardt H, Gierer A (2000) Pattern formation by local self-activation and lateral inhibition. Bioessays 22(8):753–760

    CAS  PubMed  Google Scholar 

  • Miljkovic-Licina M, Chera S, Ghila L, Galliot B (2007) Head regeneration in wild-type Hydra requires de novo neurogenesis. Development 134(6):1191–1201

    CAS  PubMed  Google Scholar 

  • Millane RC, Kanska J, Duffy DJ, Seoighe C, Cunningham S, Plickert G, Frank U (2011) Induced stem cell neoplasia in a cnidarian by ectopic expression of a POU domain transcription factor. Development 138(12):2429–2439

    CAS  PubMed  Google Scholar 

  • Miller DJ, Ball EE (2008) Cryptic complexity captured: the Nematostella genome reveals its secrets. Trends Genet 24(1):1–4

    CAS  PubMed  Google Scholar 

  • Miller MA, Technau U, Smith KM, Steele RE (2000) Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 224(2):326–338

    CAS  PubMed  Google Scholar 

  • Minguillon C, Garcia-Fernandez J (2003) Genesis and evolution of the Evx and Mox genes and the extended Hox and ParaHox gene clusters. Genome Biol 4(2):R12

    PubMed Central  PubMed  Google Scholar 

  • Mokady O, Buss LW (1996) Transmission genetics of allorecognition in Hydractinia symbiolongicarpus (Cnidaria:Hydrozoa). Genetics 143(2):823–827

    CAS  PubMed Central  PubMed  Google Scholar 

  • Momose T, Houliston E (2007) Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5(4):e70

    PubMed Central  PubMed  Google Scholar 

  • Momose T, Schmid V (2006) Animal pole determinants define oral-aboral axis polarity and endodermal cell-fate in hydrozoan jellyfish Podocoryne carnea. Dev Biol 292(2):371–380

    CAS  PubMed  Google Scholar 

  • Momose T, Derelle R, Houliston E (2008) A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135(12):2105–2113

    CAS  PubMed  Google Scholar 

  • Momose T, Kraus Y, Houliston E (2012) A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development. Development 139(23):4374–4382

    CAS  PubMed  Google Scholar 

  • Moran Y, Praher D, Fredman D, Technau U (2013) The evolution of MicroRNA pathway protein components in Cnidaria. Mol Biol Evol 30(12):2541–2552

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moran Y, Fredman D, Praher D, Li XZ, Wee LM, Rentzsch F, Zamore PD, Technau U, Seitz H (2014) Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res 24(4):651–663

    CAS  PubMed Central  PubMed  Google Scholar 

  • Müller WA (1964) Experimental investigations on colony development, polyp differentiation and sexual chimeras in Hydractinia echinata Wilhelm Roux’. Arch Entwicklungsmechanik 155:181–268

    Google Scholar 

  • Müller WA (1982) Intercalation and pattern regulation in hydroids. Differentiation 22:141–150

    Google Scholar 

  • Muller WA (1990) Ectopic head and foot formation in Hydra: diacylglycerol-induced increase in positional value and assistance of the head in foot formation. Differentiation 42(3):131–143

    CAS  PubMed  Google Scholar 

  • Muller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275(1):215–224

    PubMed  Google Scholar 

  • Muller W, Frank U, Teo R, Mokady O, Guette C, Plickert G (2007) Wnt signaling in hydroid development: ectopic heads and giant buds induced by GSK-3beta inhibitors. Int J Dev Biol 51(3):211–220

    PubMed  Google Scholar 

  • Nakanishi N, Yuan D, Hartenstein V, Jacobs DK (2010) Evolutionary origin of rhopalia: insights from cellular-level analyses of Otx and POU expression patterns in the developing rhopalial nervous system. Evol Dev 12(4):404–415

    CAS  PubMed  Google Scholar 

  • Nakanishi N, Renfer E, Technau U, Rentzsch F (2012) Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139(2):347–357

    CAS  PubMed  Google Scholar 

  • Nicotra ML, Powell AE, Rosengarten RD, Moreno M, Grimwood J, Lakkis FG, Dellaporta SL, Buss LW (2009) A hypervariable invertebrate allodeterminant. Curr Biol 19(7):583–589

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishimiya-Fujisawa C, Kobayashi S (2012) Germline stem cells and sex determination in Hydra. Int J Dev Biol 56(6–8):499–508

    PubMed  Google Scholar 

  • Nüchter T, Benoit M, Engel U, Ozbek S, Holstein TW (2006) Nanosecond-scale kinetics of nematocyst discharge. Curr Biol 16(9):R316–R318

    PubMed  Google Scholar 

  • Oliver D, Brinkmann M, Sieger T, Thurm U (2008) Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli. J Exp Biol 211(Pt 17):2876–2888

    PubMed  Google Scholar 

  • Oren M, Brikner I, Appelbaum L, Levy O (2014) Fast neurotransmission related genes are expressed in non nervous endoderm in the sea anemone Nematostella vectensis. PLoS One 9(4):e93832

    PubMed Central  PubMed  Google Scholar 

  • Ormestad M, Martindale MQ, Rottinger E (2011) A comparative gene expression database for invertebrates. EvoDevo 2:17

    PubMed Central  PubMed  Google Scholar 

  • Otto JJ (1976) Early development and planula movement in Haliclystus (Scyphozoa, Stauromedusae). In: Mackie GO (ed) Coelenterate ecology and behavior. Plenum Press, New York, pp 319–329

    Google Scholar 

  • Petie R, Garm A, Nilsson DE (2011) Visual control of steering in the box jellyfish Tripedalia cystophora. J Exp Biol 214(Pt 17):2809–2815

    PubMed  Google Scholar 

  • Philipp I, Aufschnaiter R, Ozbek S, Pontasch S, Jenewein M, Watanabe H, Rentzsch F, Holstein TW, Hobmayer B (2009) Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra. Proc Natl Acad Sci U S A 106(11):4290–4295

    PubMed Central  PubMed  Google Scholar 

  • Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Worheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19(8):706–712

    CAS  PubMed  Google Scholar 

  • Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alie A, Morgenstern B, Manuel M, Worheide G (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27(9):1983–1987

    CAS  PubMed Central  PubMed  Google Scholar 

  • Plickert G, Jacoby V, Frank U, Muller WA, Mokady O (2006) Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298(2):368–378

    CAS  PubMed  Google Scholar 

  • Plickert G, Frank U, Muller WA (2012) Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency. Int J Dev Biol 56(6–8):519–534

    PubMed  Google Scholar 

  • Poudyal M, Rosa S, Powell AE, Moreno M, Dellaporta SL, Buss LW, Lakkis FG (2007) Embryonic chimerism does not induce tolerance in an invertebrate model organism. Proc Natl Acad Sci U S A 104(11):4559–4564

    CAS  PubMed Central  PubMed  Google Scholar 

  • Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317(5834):86–94

    CAS  PubMed  Google Scholar 

  • Raikova EV (1994) Life cycle, cytology and morphology on Polypodium hydriforme, a coelenterate parasite of the eggs of acipenseriform fishes. J Parasitol 80(1):1–22

    CAS  PubMed  Google Scholar 

  • Rebscher N, Volk C, Teo R, Plickert G (2008) The germ plasm component vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev Dyn 237(6):1736–1745

    CAS  PubMed  Google Scholar 

  • Renfer E, Amon-Hassenzahl A, Steinmetz PR, Technau U (2010) A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci U S A 107(1):104–108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rentzsch F, Anton R, Saina M, Hammerschmidt M, Holstein TW, Technau U (2006) Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev Biol 296(2):375–387

    CAS  PubMed  Google Scholar 

  • Rentzsch F, Fritzenwanker JH, Scholz CB, Technau U (2008) FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135(10):1761–1769

    CAS  PubMed  Google Scholar 

  • Rosa SF, Powell AE, Rosengarten RD, Nicotra ML, Moreno MA, Grimwood J, Lakkis FG, Dellaporta SL, Buss LW (2010) Hydractinia allodeterminant alr1 resides in an immunoglobulin superfamily-like gene complex. Curr Biol 20(12):1122–1127

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5(5):355–362

    CAS  PubMed  Google Scholar 

  • Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2(4):500–506

    PubMed  Google Scholar 

  • Rosengarten RD, Moreno MA, Lakkis FG, Buss LW, Dellaporta SL (2011) Genetic diversity of the allodeterminant alr2 in Hydractinia symbiolongicarpus. Mol Biol Evol 28(2):933–947

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rottinger E, Dahlin P, Martindale MQ (2012) A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specification: the inputs of ss-catenin/TCF signaling. PLoS Genet 8(12):e1003164

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruzickova J, Piatigorsky J, Kozmik Z (2009) Eye-specific expression of an ancestral jellyfish PaxB gene interferes with Pax6 function despite its conserved Pax6/Pax2 characteristics. Int J Dev Biol 53(4):469–482

    CAS  PubMed  Google Scholar 

  • Ryan JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, Martindale MQ, Finnerty JR (2007) Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS One 2(1):e153

    PubMed Central  PubMed  Google Scholar 

  • Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Program NCS, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342(6164):1242592

    PubMed Central  PubMed  Google Scholar 

  • Saina M, Genikhovich G, Renfer E, Technau U (2009) BMPs and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci U S A 106(44):18592–18597

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sarras MP Jr (2012) Components, structure, biogenesis and function of the Hydra extracellular matrix in regeneration, pattern formation and cell differentiation. Int J Dev Biol 56(6–8):567–576

    CAS  PubMed  Google Scholar 

  • Sato M, Bode HR, Sawada Y (1990) Patterning processes in aggregates of Hydra cells visualized with the monoclonal antibody, TS19. Dev Biol 141(2):412–420

    CAS  PubMed  Google Scholar 

  • Schaller H, Gierer A (1973) Distribution of the head-activating substance in Hydra and its localization in membranous particles in nerve cells. J Embryol Exp Morphol 29(1):39–52

    CAS  PubMed  Google Scholar 

  • Schaller HC, Hofmann M, Javois LC (1990) Effect of head activator on proliferation, head-specific determination and differentiation of epithelial cells in Hydra. Differentiation 43(3):157–164

    CAS  PubMed  Google Scholar 

  • Schmich J, Trepel S, Leitz T (1998) The role of GLWamides in metamorphosis of Hydractinia echinata. Dev Genes Evol 208(5):267–273

    CAS  PubMed  Google Scholar 

  • Schmid V, Alder H (1984) Isolated, mononucleated, striated muscle can undergo pluripotent transdifferentiation and form a complex regenerate. Cell 38(3):801–809

    CAS  PubMed  Google Scholar 

  • Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci 85:197–215

    CAS  PubMed  Google Scholar 

  • Scholz CB, Technau U (2003) The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 212(12):563–570

    CAS  PubMed  Google Scholar 

  • Schwaiger M, Schonauer A, Rendeiro AF, Pribitzer C, Schauer A, Gilles AF, Schinko JB, Renfer E, Fredman D, Technau U (2014) Evolutionary conservation of the eumetazoan gene regulatory landscape. Genome Res 24(4):639–650

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seipel K, Schmid V (2005) Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev Biol 282(1):14–26

    CAS  PubMed  Google Scholar 

  • Seipel K, Yanze N, Schmid V (2004) Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish. Dev Biol 269(2):331–345

    CAS  PubMed  Google Scholar 

  • Seipp S, Schmich J, Kehrwald T, Leitz T (2007) Metamorphosis of Hydractinia echinata–natural versus artificial induction and developmental plasticity. Dev Genes Evol 217(5):385–394

    PubMed  Google Scholar 

  • Seipp S, Schmich J, Will B, Schetter E, Plickert G, Leitz T (2010) Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa). Invert Neurosci 10(2):77–91

    CAS  PubMed  Google Scholar 

  • Shimizu H (2012) Transplantation analysis of developmental mechanisms in Hydra. Int J Dev Biol 56(6–8):463–472

    PubMed  Google Scholar 

  • Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476(7360):320–323

    CAS  PubMed  Google Scholar 

  • Spring J, Yanze N, Middel AM, Stierwald M, Groger H, Schmid V (2000) The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228(2):363–375

    CAS  PubMed  Google Scholar 

  • Spring J, Yanze N, Josch C, Middel AM, Winninger B, Schmid V (2002) Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of Bilateria. Dev Biol 244(2):372–384

    CAS  PubMed  Google Scholar 

  • Squire JM, Al-Khayat HA, Knupp C, Luther PK (2005) Molecular architecture in muscle contractile assemblies. Adv Protein Chem 71:17–87. doi:10.1016/S0065-3233(04)71002-5

    CAS  PubMed  Google Scholar 

  • Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454(7207):955–960

    CAS  PubMed  Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–726

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stangl K, Salvini-Plawen L, Holstein TW (2002) Staging and induction of medusa metamorphosis in Carybdea marsupialis (Cnidaria, Cubozoa). Vie Mileu 52:131–140

    Google Scholar 

  • Steinmetz PR, Kraus JE, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Worheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487(7406):231–234

    CAS  PubMed Central  PubMed  Google Scholar 

  • Straehler-Pohl I, Jarms G (2005) Life cycle of Carybdea marsupialis Linnaeus, 1758 (Cubozoa, Carybdeidae) reveals metamorphosis to be a modified strobilation. Mar Biol 147:1271–1277

    Google Scholar 

  • Suga H, Schmid V, Gehring WJ (2008) Evolution and functional diversity of jellyfish opsins. Curr Biol 18(1):51–55

    CAS  PubMed  Google Scholar 

  • Suga H, Tschopp P, Graziussi DF, Stierwald M, Schmid V, Gehring WJ (2010) Flexibly deployed Pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish. Proc Natl Acad Sci U S A 107(32):14263–14268

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi T (2013) Neuropeptides and epitheliopeptides: structural and functional diversity in an ancestral metazoan Hydra. Protein Pept Lett 20(6):671–680

    CAS  PubMed  Google Scholar 

  • Takahashi T, Fujisawa T (2009) Important roles for epithelial cell peptides in Hydra development. Bioessays 31(6):610–619

    CAS  PubMed  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676

    CAS  PubMed  Google Scholar 

  • Tardent P (1978) Coelenterata, Cnidaria. Morphogenese der Tiere. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Technau U (2001) Brachyury, the blastopore and the evolution of the mesoderm. Bioessays 23(9):788–794

    CAS  PubMed  Google Scholar 

  • Technau U, Bode HR (1999) HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development 126(5):999–1010

    CAS  PubMed  Google Scholar 

  • Technau U, Holstein TW (1992) Cell sorting during the regeneration of Hydra from reaggregated cells. Dev Biol 151(1):117–127

    CAS  PubMed  Google Scholar 

  • Technau U, Holstein TW (1995a) Boundary cells of endodermal origin define the mouth of Hydra vulgaris (Cnidaria). Cell Tissue Res 280:235–242

    Google Scholar 

  • Technau U, Holstein TW (1995b) Head formation is different at apical and basal levels. Development 121:1273–1282

    CAS  Google Scholar 

  • Technau U, Holstein TW (1996) Phenotypic maturation of neurons and continuous precursor migration in the formation of the peduncle nerve net in Hydra. Dev Biol 177(2):599–615

    CAS  PubMed  Google Scholar 

  • Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: cnidaria. Development 138(8):1447–1458

    Google Scholar 

  • Technau U, Cramer von Laue C, Rentzsch F, Luft S, Hobmayer B, Bode HR, Holstein TW (2000) Parameters of self-organization in Hydra aggregates. Proc Natl Acad Sci U S A 97(22):12127–12131

    CAS  PubMed Central  PubMed  Google Scholar 

  • Technau U, Miller MA, Bridge D, Steele RE (2003) Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev Biol 260(1):191–206

    CAS  PubMed  Google Scholar 

  • Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21(12):633–639

    CAS  PubMed  Google Scholar 

  • Teo R, Mohrlen F, Plickert G, Muller WA, Frank U (2006) An evolutionary conserved role of Wnt signaling in stem cell fate decision. Dev Biol 289(1):91–99

    CAS  PubMed  Google Scholar 

  • Thomas-Chollier M, Ledent V, Leyns L, Vervoort M (2010) A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution. BMC Evol Biol 10:73

    PubMed Central  PubMed  Google Scholar 

  • Turing A (1952) The chemical basis for morphogenesis. Phil Trans R Soc B 237:37–72

    Google Scholar 

  • Watanabe H, Hoang VT, Mattner R, Holstein TW (2009) Immortality and the base of multicellular life: lessons from cnidarian stem cells. Semin Cell Dev Biol 20(9):1114–1125

    CAS  PubMed  Google Scholar 

  • Weber J (1990) Poly(gamma-glutamic acid)s are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J Biol Chem 265(17):9664–9669

    CAS  PubMed  Google Scholar 

  • Weill R (1934) Contribution à l’étude des cnidaires et leurs nematocystes. Trav Stat Zool Wimereux 10–11:1–700

    Google Scholar 

  • Wietrzykowski W (1910) Sur le développement des Lucernaridés (note préliminaire). Arch Zool Exp 2:10–27

    Google Scholar 

  • Wietrzykowski W (1912) Recherches sur le développement des Lucernaires. Arch Zool Exp Gen 10:1–95

    Google Scholar 

  • Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ (2003) An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426(6965):446–450

    CAS  PubMed  Google Scholar 

  • Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F, Bosch TC (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci U S A 103(16):6208–6211

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP (1999) T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13(24):3185–3190

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zenkert C, Takahashi T, Diesner MO, Ozbek S (2011) Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS One 6(7):e22725

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

We thank the members of the Technau lab for continuous fruitful discussions. We especially thank Andy Aman for critically reading and correcting the manuscript. Also, we wish to acknowledge the Core Facility Cell Imaging and Ultrastructure Research for support in confocal imaging. Work in the Technau lab is supported by grants of the Austrian Science Fund FWF to UT and GG (P24858; P22618; P26962).

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Authors and Affiliations

  1. Department of Molecular Evolution and Development, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, Wien, 1090, Austria

    Ulrich Technau, Grigory Genikhovich & Johanna E. M. Kraus

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  1. Ulrich Technau
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  2. Grigory Genikhovich
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  3. Johanna E. M. Kraus
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Correspondence to Ulrich Technau .

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  1. Department of Integrative Zoology, University of Vienna Faculty of Life Sciences, Wien, Austria

    Andreas Wanninger

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Technau, U., Genikhovich, G., Kraus, J.E.M. (2015). Cnidaria. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 1. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1862-7_6

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