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The rise of the starlet sea anemone Nematostella vectensis as a model system to investigate development and regeneration

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Michael J. Layden, Fabian Rentzsch, Eric Röttinger

Published Online: Feb 19 2016

DOI: 10.1002/wdev.222

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Reverse genetics and next‐generation sequencing unlocked a new era in biology. It is now possible to identify an animal(s) with the unique biology most relevant to a particular question and rapidly generate tools to functionally dissect that biology. This review highlights the rise of one such novel model system, the starlet sea anemone Nematostella vectensis. Nematostella is a cnidarian (corals, jellyfish, hydras, sea anemones, etc.) animal that was originally targeted by EvoDevo researchers looking to identify a cnidarian animal to which the development of bilaterians (insects, worms, echinoderms, vertebrates, mollusks, etc.) could be compared. Studies in Nematostella have accomplished this goal and informed our understanding of the evolution of key bilaterian features. However, Nematostella is now going beyond its intended utility with potential as a model to better understand other areas such as regenerative biology, EcoDevo, or stress response. This review intends to highlight key EvoDevo insights from Nematostella that guide our understanding about the evolution of axial patterning mechanisms, mesoderm, and nervous systems in bilaterians, as well as to discuss briefly the potential of Nematostella as a model to better understand the relationship between development and regeneration. Lastly, the sum of research to date in Nematostella has generated a variety of tools that aided the rise of Nematostella to a viable model system. We provide a catalogue of current resources and techniques available to facilitate investigators interested in incorporating Nematostella into their research. WIREs Dev Biol 2016, 5:408–428. doi: 10.1002/wdev.222 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan Comparative Development and Evolution > Model Systems Technologies > Perturbing Genes and Generating Modified Animals

Nematostella vectensis is an anthozoan cnidarian sea anemone. (a) Image of adult Nematostella polyp. Image taken by Eric Röttinger. (b) Phylogeny showing the sister relationship of cnidarians to bilaterians and Nematostella's position within the cnidarians.

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Diagram summarizing the morphological and cellular events underlying Nematostella oral regeneration. The table below the illustration provides definitions for the various regeneration steps. *, mouth opening; ten, tentacles; ten bud, tentacle bud; pha, pharynx; pha lip, pharyngeal lip; mes, mesenteries. (Reprinted with permission from Ref . Copyright 2015 International Journal of Molecular Sciences)

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Oral regeneration of juvenile Nematostella takes place in 6 days. After sub‐pharyngeal bisection, missing oral part of the polyps regenerate within 6 days to reform a fully functional organism. Animals were fixed and stained with phalloidin (green) to show f‐actin filaments and propidium iodide (red) to visualize the nuclei. All images are lateral views with the oral part to the top.

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Morphology of Nematostella nervous system in juvenile polyps. (a, b) 3D reconstruction of confocal Z‐series acquired for two Nematostella transgenic lines that label the nervous system (a) NvElav::mOrange and (b) NvLWamide::mCherry. (c) Schematic of juvenile polyp nervous system highlights key structures and provides examples of neuronal morphologies observed in transgenic animals.

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Development and morphology of Nematostella. (a) Schematic of Nematostella developmental stages. Modified from Ormestad et al. Ref . Orange represents presumptive endoderm in blastula and the endoderm in all subsequent stages. The outer ectoderm is white, and the aboral ectodermal domain is in light blue. (b) DIC image taken by Aldine Amiel of juvenile polyp. The mouth (oral opening) is indicated by (Or), the tentacles by (tent), the pharynx by (Ph), and the mesenteries by (mes). Oral is up in all images.

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(GRN) Co‐expression domains within the animal hemisphere of the Nematostella blastula. (a, b) Diagram illustrating four co‐expression domains within the animal hemisphere defined by differential spatial expression of the genes indicated in (b). (c) Examples of genes expression in either the central ring (NvsnailA), the central domain (NvfoxB), the central domain + ring (NvashB), or the external ring (Nvwnt4). In situ hybridization expression profiles are shown in either lateral view (a, top row of c) or animal view (b, bottom row of c) to distinguish expression domains. (Reprinted with permission from Ref . Copyright 2012 PLoS Genetics)

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Gene expression during axial patterning. Localization of transcripts (in italic) and proteins involved in the patterning of the oral–aboral (a) and directive (b) axis, respectively. The developmental stages are indicated above each cartoon. Note that not all details of the expression patterns are captured. In (a), the expression domain of wnt4 is broader than that of wntA and wnt1. frizzled5/8 is at planula stage strongly expressed at the aboral pole (green) and weakly in a broader aboral domain (pink). hoxF/anthox1 is at planula stage expressed in the small aboral pole domain (green) and in individual cells within the broader aboral domain (pink). It is not clear whether the expression domains depicted in blue, yellow, and pink are directly abutting each other. In the zygote, Disheveled protein is localized at the cortex and around the nucleus. Disheveled and Strabismus protein remain preferentially localized to the animal/blastoporal region at least until gastrula stage. In (b), BMP5‐8 is at gastrula stage co‐expressed in the ectoderm with bmp2/4, chordin, and rgm (i.e., the domain in light green). pSmad1/5/8 staining forms a gradient with highest levels on the side opposite to the bmp expressing side and low levels on the bmp expressing side. See main text for references.

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References

Dunn, CW, Hejnol A, Matus MQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745–749.
Ryan, JF, Pang K, Schnitzler CE, Nguyen A, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, et al. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 2013, 342:1242592.
Hejnol, A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc B Biol Sci 2009, 276:4261–4270.
Hand, C, Uhlinger, KR. The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 1992, 182:169–176.
Houliston, E, Momose, T, Manuel, M. Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 2015, 26:159–167.
Plickert, G, Frank, U, Müller, WA. Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency. Int J Dev Biol 2012, 56:519–534.
Fritzenwanker, JH, Genikhovich, G, Kraus, Y, Technau, U. Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol 2007, 310:264–279.
Lee, PN, Kumburegama, S, Marlow, HQ, Martindale, MQ, Wikramanayake, AH. Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol 2007, 310:169–186.
Fritzenwanker, JH, Technau, U. Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 2002, 212:99–103.
Stefanik, DJ, Friedman, LE, Finnerty, JR. Collecting, rearing, spawning and inducing regeneration of the starlet sea anemone, Nematostella vectensis. Nat Protoc 2013, 8:916–923.
Fritz, AE, Ikmi, A, Seidel, C, Paulson, A, Gibson, MC. Mechanisms of tentacle morphogenesis in the sea anemone Nematostella vectensis. Development 2013, 140:2212–2223.
Renfer, E, Amon‐Hassenzahl, A, Steinmetz, PRH, Technau, U. A muscle‐specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci USA 2010, 107:104–108.
Extavour, CG, Pang, K, Matus, DQ, Martindale, MQ. vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol Dev 2005, 7:201–215.
Tucker, RP, Shibata, B, Blankenship, TN. Ultrastructure of the mesoglea of the sea anemone Nematostella vectensis (Edwardsiidae). Invertebr Biol 2011, 130:11–24.
Leclère, L, Rentzsch, F. RGM regulates BMP‐mediated secondary axis formation in the sea anemone Nematostella vectensis. Cell Rep 2014, 9:1921–1930. doi:10.1016/j.celrep.2014.11.009.
Berking, S. Generation of bilateral symmetry in Anthozoa: a model. J Theor Biol 2007, 246:477–490.
Zenkert, C, Takahashi, T, Diesner, M‐O, Ozbek, S. Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS One 2011, 6:e22725.
Marlow, HQ, Srivastava, M, Matus, DQ, Rokhsar, D, Martindale, MQ. Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol 2009, 69:235–254.
Layden, MJ, Boekhout, M, Martindale, MQ. Nematostella vectensis achaete‐scute homolog NvashA regulates embryonic ectodermal neurogenesis and represents an ancient component of the metazoan neural specification pathway. Development 2012, 139:1013–1022.
Sinigaglia, C, Busengdal, H, Leclère, L, Technau, U, Rentzsch, F. The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol 2013, 11:e1001488.
Nakanishi, N, Renfer, E, Technau, U, Rentzsch, F. Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 2011, 139:347–357.
Kusserow, A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, et al. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 2005, 433:156–160.
Putnam, NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86–94.
Varmuza, S, Sullivan, JC, Finnerty, JR. A surprising abundance of human disease genes in a simple ‘basal’ animal, the starlet sea anemone (Nematostella vectensis). Genome 2007, 50:689–692.
Grimson, ASrivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. Early origins and evolution of microRNAs and Piwi‐interacting RNAs in animals. Nature 2008, 455:1193–1197.
Moran, Y, Fredman D, Praher D, Li XZ, Wee LM, Rentzsch F, Zamore PD, Technau U, Seitz H. Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res 2014, 24:651–663.
Schwaiger, M, Schönauer, A, Rendeiro, AF, Pribitzer, C, Schauer, A, Gilles, AF, Schinko, JB, Renfer, E, Fredman, D, Technau, U. Evolutionary conservation of the eumetazoan gene regulatory landscape. Genome Res 2014, 24:639–650.
Helm, RR, Siebert, S, Tulin, S, Smith, J, Dunn, CW. Characterization of differential transcript abundance through time during Nematostella vectensis development. BMC Genomics 2013, 14:266.
Tulin, S, Aguiar, D, Istrail, S, Smith, J. A quantitative reference transcriptome for Nematostella vectensis early embryonic development: a pipeline for de novo assembly in emerging model systems. Evodevo 2013, 4:16.
Genikhovich, G, Technau, U. Complex functions of Mef2 splice variants in the differentiation of endoderm and of a neuronal cell type in a sea anemone. Development 2011, 138:4911–4919.
Genikhovich, G, Technau, U. The starlet sea anemone Nematostella vectensis: an anthozoan model organism for studies in comparative genomics and functional evolutionary developmental biology. Cold Spring Harb Protoc 2009, 2009:pdb.emo129.
Amiel, AR, Johnston, HT, Nedoncelle, K, Warner, JF, Ferreira, S, Röttinger, E. Characterization of morphological and cellular events underlying oral regeneration in the sea anemone, Nematostella vectensis. Int J Mol Sci 2015, 16:28449–28471.
DuBuc, TQ, Traylor‐Knowles, N, Martindale, MQ. Initiating a regenerative response, cellular and molecular features of wound healing in the cnidarian Nematostella vectensis. BMC Biol 2014, 214:134–138.
Bossert, PE, Dunn, MP, Thomsen, GH. A staging system for the regeneration of a polyp from the aboral physa of the anthozoan cnidarian Nematostella vectensis. Dev Dyn 2013, 242:1320–1331.
Ikmi, A, McKinney, SA, Delventhal, KM, Gibson, MC. TALEN and CRISPR/Cas9‐mediated genome editing in the early‐branching metazoan Nematostella vectensis. Nat Commun 2014, 5:5486.
Magie, CR, Daly, M, Martindale, MQ. Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression. Dev Biol 2007, 305:483–497.
Rentzsch, F, Fritzenwanker, JH, Scholz, CB, Technau, U. FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 2008, 135:1761–1769.
Layden, MJ, Röttinger, E, Wolenski, FS, Gilmore, TD, Martindale, MQ. Microinjection of mRNA or morpholinos for reverse genetic analysis in the starlet sea anemone, Nematostella vectensis. Nat Protoc 2013, 8:924–934.
Wikramanayake, AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ. An ancient role for nuclear β‐catenin in the evolution of axial polarity and germ layer segregation. Nature 2003, 426:446–450.
Röttinger, E, Dahlin, P, Martindale, MQ. A framework for the establishment of a cnidarian gene regulatory network for ‘endomesoderm’ specification: the inputs of β‐catenin/TCF signaling. PLoS Genet 2012, 8:e1003164.
Sinigaglia, C, Busengdal, H, Lerner, A, Oliveri, P, Rentzsch, F. Molecular characterization of the apical organ of the anthozoan Nematostella vectensis. Dev Biol 2015, 398:120–133.
Wolenski, FS, Layden, MJ, Martindale, MQ, Gilmore, TD, Finnerty, JR. Characterizing the spatiotemporal expression of RNAs and proteins in the starlet sea anemone, Nematostella vectensis. Nat Protoc 2013, 8:900–915.
Freeman, G. The role of polarity in the development of the hydrozoan planula larva. Roux`s Arch Dev Biol 1981, 190:168–184.
Finnerty, JR. Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 2004, 304:1335–1337.
Ryan, JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, Martindale MQ, Finnerty JR. Pre‐bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS One 2007, 2:e153.
Kamm, K, Schierwater, B, Jakob, W, Dellaporta, SL, Miller, DJ. Axial patterning and diversification in the cnidaria predate the Hox system. Curr Biol 2006, 16:920–926.
Chiori, R et al. Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (cnidaria). PLoS One 2009, 4:e4231.
Quiquand, M et al. More constraint on ParaHox than Hox gene families in early metazoan evolution. Dev Biol 2009, 328:173–187.
Yanze, N, Spring, J, Schmidli, C, Schmid, V. Conservation of Hox/ParaHox‐related genes in the early development of a cnidarian. Dev Biol 2001, 236:89–98.
Kumburegama, S, Wijesena, N, Xu, R, Wikramanayake, AH. 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. Evodevo 2011, 2:2.
Lee, PN, Pang, K, Matus, DQ, Martindale, MQ. A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 2006, 17:157–167.
Marlow, H, Matus, DQ, Martindale, MQ. 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 2013, 380:324–334.
Momose, T, Houliston, E. Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 2007, 5:e70.
Momose, T, Derelle, R, Houliston, E. A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. %3EDevelopment 2008, 135:2105–2113.
Plickert, G, Jacoby, V, Frank, U, Müller, WA, Mokady, O. Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 2006, 298:368–378.
Schmidt‐Rhaesa,, A. The Evolution of Organs Systems. Oxford, UK: Oxford University Press; 2007.
Galliot, B, Miller, DJ. Origin of anterior patterning: how old is our head? Trends Genet 2000, 16:1–5.
Aronowicz, J, Lowe, CJ. Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems. Integr Comp Biol 2006, 46:890–901.
Darras, S, Gerhart, J, Terasaki, M, Kirschner, M, Lowe, CJ. Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 2011, 138:959–970.
Wei, Z, Yaguchi, J, Yaguchi, S, Angerer, RC, Angerer, LM. The sea urchin animal pole domain is a Six3‐dependent neurogenic patterning center. Development 2009, 136:1179–1189.
Tu, Q, Brown, CT, Davidson, EH, Oliveri, P. Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 2006, 300:49–62.
Santagata, S, Resh, C, Hejnol, A, Martindale, MQ, Passamaneck, YJ. Development of the larval anterior neurogenicdomains of Terebratalia transversa (Brachiopoda) provides insights into the diversification of larvalapical organs and the spiralian nervous system. Evodevo 2012, 3:3.
Carlgren, O. Studien ueber Nordische Actinien. Vetenskap‐Akademiens Handlinger 1893, 25:1–148.
Hyman,, L. The Invertebrates: Protozoa through Ctenophora. New York: McGraw‐Hill; 1940, 538–565.
Matus, DQ, Thomsen, GH, Martindale, MQ. Dorso/ventral genes are asymmetrically expressed and involved in germ‐layer demarcation during cnidarian gastrulation. Curr Biol 2006, 16:499–505.
Matus, DQ, Pang, K, Marlow, H, Dunn, CW, Thomsen, GH, Martindale, MQ. Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci USA 2006, 103:11195–11200.
Hayward, DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE. Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci USA 2002, 99:8106–8111.
Rentzsch, F, Anton R, Saina M, Hammerschmidt M, Holstein TW, Technau U. Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev Biol 2006, 296:375–387.
Saina, M, Genikhovich, G, Renfer, E, Technau, U. BMPs and Chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci 2009, 106:18582–18597. doi:10.1073/pnas.0900151106.
Genikhovich, G et al. Axis patterning by BMPs: cnidarian network reveals evolutionary constraints. Cell Rep 2015, 10:1646–1654.
Cameron, RA, Davidson, EH. Cell type specification during sea urchin development. Trends Genet 1991, 7:212–218.
Rodaway, A, Patient, R. Mesendoderm: an ancient germ layer? Cell 2001, 105:169–172.
Kimelman, D, Griffin, KJ. Vertebrate mesendoderm induction and patterning. Curr Opin Genet Dev 2000, 10:350–356.
Martindale, MQ. Investigating the origins of triploblasty: ‘mesodermal` gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 2004, 131:2463–2474.
Martindale, MQ. The evolution of metazoan axial properties. Nat Rev Genet 2005, 6:917–927.
Martindale,, M. Q. & Finnerty,, J. R. The Radiata and the evolutionary origins of the bilaterian body plan. Mol Phylogenet Evol 2002, 24: 358–365.
Seipel, K, Schmid, V. Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 2006, 50:589–599.
Scholz, CB, Technau, U. The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 2003, 212:563–570.
Technau, U. Brachyury, the blastopore and the evolution of the mesoderm. Bioessays 2001, 23:788–794.
Burton, PM. Insights from diploblasts; the evolution of mesoderm and muscle. J Exp Zool 2007, 310B:5–14.
Byrum, CA, Martindale, MQ. Gastrulation. From Cells to Embryo. Cold Spring Harbor, NY: Cold Spring Harbor Press; 2004, 33–50.
Jahnel,, SM., Walzl,, M. & Technau,, U. Development and epithelial organisation of muscle cells in the sea anemone Nematostella vectensis Front Zool 11, 44 (2014).
Mazza, ME, Pang, K, Martindale, MQ, Finnerty, JR. Genomic organization, gene structure, and developmental expression of three Clustered otx genes in the sea anemone Nematostella vectensis. J Exp Zool 2007, 308B:494–506.
Davidson, EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, et al. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev Biol 2002, 246:162–190.
Vonica, A, Weng, W, Gumbiner, BM, Venuti, JM. TCF is the nuclear effector of the β‐catenin signal that patterns the sea urchin animal–vegetal axis. Dev Biol 2000, 217:230–243.
Imai, K, Takada, N, Satoh, N, Satou, Y. β‐Catenin mediates the specification of endoderm cells in ascidian embryos. Development 2000, 127:3009–3020.
Schohl, A, Fagotto, F. A role for maternal‐catenin in early mesoderm induction in Xenopus. EMBO J 2003, 22:3303–3313.
Huang, L, Li X, El-Hodiri M, Dayal S, Wikramanayake AH, Klein WH. Involvement of Tcf/Lef in establishing cell types along the animal‐vegetal axis of sea urchins. Dev Genes Evol 2000, 210:73–81.
Matus, DQ, Magie, CR, Pang, K, Martindale, MQ, Thomsen, GH. The Hedgehog gene family of the cnidarian, Nematostella vectensis, and implications for understanding metazoan Hedgehog pathway evolution. Dev Biol 2008, 313:501–518.
Fritzenwanker, JH, Saina, M, Technau, U. Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 2004, 275:389–402.
Ormestad, M, Martindale, MQ, Röttinger, E. A comparative gene expression database for invertebrates. Evodevo 2011, 2:17.
Botman, D, Kaandorp, JA. Spatial gene expression quantification: a tool for analysis of in situ hybridizations in sea anemone Nematostella vectensis. BMC Res Notes 2012, 5:555.
Botman, D, Röttinger, E, Martindale, MQ, de Jong, J, Kaandorp, JA. A Computational approach towards a gene regulatory network for the developing Nematostella vectensis gut. PLoS One 2014, 9:e103341.
Loose, M, Patient, R. A genetic regulatory network for Xenopus mesendoderm formation. Dev Biol 2004, 271:467–478.
Hinman, VF, Nguyen, A, Davidson, EH. Caught in the evolutionary act: precise cis‐regulatory basis of difference in the organization of gene networks of sea stars and sea urchins. Dev Biol 2007, 312:584–595.
Hinman, VF, Nguyen, AT, Davidson, EH. Expression and function of a starfish Otx ortholog, AmOtx: a conserved role for Otx proteins in endoderm development that predates divergence of the eleutherozoa. Mech Dev 2003, 120:1165–1176.
Oliveri, P, Walton, KD, Davidson, EH, McClay, DR. Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 2006, 133:4173–4181.
Ghysen, A. The origin and evolution of the nervous system. Int J Dev Biol 2003, 47:555–562.
Watanabe, H, Fujisawa, T, Holstein, TW. Cnidarians and the evolutionary origin of the nervous system. Dev Growth Differ 2009, 51:167–183.
Moran, Y, Genikhovich G, Gordon D, Wienkoop S, Zenkert C, Özbeck S, Technau U, Gurevitz M. Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones. Proc R Soc B Biol Sci 2012, 279:1351–1358.
Kass‐Simon, G, Scappaticci, AA Jr. The behavioral and developmental physiology of nematocysts. Can J Zool 2002, 80:1772–1794.
Watanabe, H, Kuhn A, Fushiki M, Agata K, Özbek S, Fujisawa T, Holstein TW. Sequential actions of β‐catenin and Bmp pattern the oral nerve net in Nematostella vectensis. Nat Commun 2014, 5:1–14.
Richards, GS, Rentzsch, F. Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis. Development 2014, 141:4681–4689.
Bertrand, N, Castro, DS, Guillemot, F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 2002, 3:517–530.
Simionato, E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M. Origin and diversification of the basic helix‐loop‐helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 2007, 7:33.
Zhao, G, Skeath, JB. The Sox‐domain containing gene Dichaete/fish‐hook acts in concert with vnd and ind to regulate cell fate in the Drosophila neuroectoderm. Development 129: 1165–1174 (2002).
Graham, V, Khudyakov, J, Ellis, P, Pevny, L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39:749–765.
Sandberg, M, Källström, M, Muhr, J. Sox21 promotes the progression of vertebrate neurogenesis. Nat Neurosci 2005, 8:995–1001.
Jager, M, Quéinnec, E, Le Guyader, H, Manuel, M. Multiple Sox genes are expressed in stem cells or in differentiating neuro‐sensory cells in the hydrozoan Clytia hemisphaerica. Evodevo 2011, 2:12.
Magie, CR, Pang, K, Martindale, MQ. Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 2005, 215:618–630.
Marlow, H, Roettinger, E, Boekhout, M, Martindale, MQ. Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev Biol 2012, 362:295–308. doi:10.1016/j.ydbio.2011.11.012.
Layden, MJ, Martindale, MQ. Non‐canonical Notch signaling represents an ancestral mechanism to regulate neural differentiation. Evodevo 2014, 5:30.
Matus, DQ, Thomsen, GH, Martindale, MQ. FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. Dev Genes Evol 2007, 217:137–148.
Marlow, H et al. Larval body patterning and apical organs are conserved in animal evolution. BMC Biol 2014, 12:1–17.
Nielsen, C. Larval and adult brains. Evol Dev 2005, 7:483–489.
Martindale, MQ, Hejnol, A. A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev Cell 2009, 17:162–174.
Binari, LA, Lewis, GM, Kucenas, S. Perineurial glia require notch signaling during motor nerve development but not regeneration. J Neurosci 2013, 33:4241–4252.
Nacu, E, Tanaka, EM. Limb regeneration: a new development? Annu Rev Cell Dev Biol 2011, 27:409–440.
Carlson, MRJ, Komine, Y, Bryant, SV, Gardiner, DM. Expression of Hoxb13 and Hoxc10 in developing and regenerating Axolotl limbs and tails. Dev Biol 2001, 229:396–406.
Gemberling, M, Bailey, TJ, Hyde, DR, Poss, KD. The zebrafish as a model for complex tissue regeneration. Trends Genet 2013, 29:611–620.
Passamaneck, YJ, Martindale, MQ. Cell proliferation is necessary for the regeneration of oral structures in the anthozoan cnidarian Nematostella vectensis. BMC Dev Biol 2012, 12:34.
Darling, JA et al. Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 2005, 27:211–221.
Reitzel, AM, Burton, PM, Krone, C, Finnerty, JR. Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission. Invertebr Biol 2007, 126:99–112.
Burton, PM, Finnerty, JR. Conserved and novel gene expression between regeneration and asexual fission in Nematostella vectensis. Dev Genes Evol 2009, 219:79–87.
Trevino, M, Stefanik, DJ, Rodriguez, R, Harmon, S, Burton, PM. Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis. Dev Dyn 2011, 240:2673–2679.
Käsbauer, T et al. The Notch signaling pathway in the cnidarian Hydra. Dev Biol 2007, 303:376–390.

Further Reading

Rigo‐Watermeier, T et al. Functional conservation of Nematostella Wnts in canonical and noncanonical Wnt‐signaling. Biol Open 2012, 1:43–51.

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