Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
, 138 (8), 1447-58

Evolutionary Crossroads in Developmental Biology: Cnidaria

Affiliations
Review

Evolutionary Crossroads in Developmental Biology: Cnidaria

Ulrich Technau et al. Development.

Abstract

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.

Figures

Fig. 1.
Fig. 1.
Phylogenetic relationships of classes in the phylum Cnidaria. A phylogenetic tree [based on the results of Collins (Collins, 2002) and Collins et al. (Collins et al., 2006)] showing the relationships within the phylum Cnidaria. The two main divisions of Cnidaria (Anthozoa and Medusozoa) are indicated in red. Anthozoa is a class that contains two subclasses (green), whereas Medusozoa is a subphylum consisting of four classes (green). Sequenced genomes (pink) are available for Nematostella and Hydra (Chapman et al., 2010; Putnam et al., 2007), whereas the genomes of Acropora and Clytia are currently being sequenced (black).
Fig. 2.
Fig. 2.
Life cycles of the main cnidarian model systems. (A,B) Anthozoan polyps either burrow into the soft substrate (A), here exemplified by the edwardsiid sea anemone Nematostella vectensis, or are attached to the surface (B), as with many sea anemones and corals, here exemplified by Acropora millepora. Nematostella female polyps release packages of several hundred eggs into the water, where they are fertilized (Fritzenwanker and Technau, 2002; Hand and Uhlinger, 1992). The resulting embryos develop into ciliated planula larvae that undergo either a gradual (Nematostella) or more dramatic (Acropora) metamorphosis into a sessile primary polyp, which involves calcification and formation of the skeleton in corals. (C) In Hydra, gametes develop from interstitial stem cells located in the ectoderm that differentiate within several testes or within a single egg patch. The embryo remains attached to the parent polyp from fertilization through gastrulation. The postgastrula embryo forms a cuticle from which the primary polyp hatches after several weeks or months. (D) The hydrozoan Clytia hemisphaerica forms a colony with feeding polyps (autozooids) and medusae-bearing gonozooids. Gametes are released from the medusae into the water. The embryo develops into a planula larva that settles to transform into a primary polyp, which then forms a new colony. Drawings are by Hanna Kraus (A,B,D) or modified from Tardent (Tardent, 1978) with permission (C).
Fig. 3.
Fig. 3.
Cnidarian model systems used in developmental biology. (A-C) Nematostella vectensis, showing adult polyp (A), planula larva (B) and primary polyp (C). (D,E) Acropora millepora showing coral (D) and planula larva and metamorphosing early settlement stages (E). (F-H) Hydra vulgaris showing budding polyp (F), cuticle stage postgastrula embryo (G) and hatching primary polyp (H). (I-K) Clytia hemisphaerica showing autozooid and gonozooid polyps (I), young medusa (J) and planula larva (K). Note the differences in size between different cnidarians. All polyps and planulae are oriented with oral side up (except for A). Images were taken by Jens Fritzenwanker and U.T. (A-C), David Miller (D), Eldon Ball (E), Tim Nüchter and Thomas Holstein (F), U.T. (G,H) and Hanna Kraus and U.T. (I-K). The images in B and C are reproduced with permission (Rentzsch et al., 2008). Scale bars: 1 cm in A; 70 μm in B,K; 80 μm in C; 5 cm in D; 150 μm in E; 500 μm in F,J; 250 μm in G,H; 100 μm in I.
Fig. 4.
Fig. 4.
Anatomy of a hydrozoan polyp. (A) A Hydra polyp is essentially a two-layered tube, with a ring of tentacles around the mouth opening at the tip of the hypostome. Asexual budding occurs on the lower half of the body column. Interstitial stem cells and nematoblasts are distributed evenly in the body column, below the tentacle ring and above the border of the peduncle, which is the stalk between the budding region and pedal disc. (B) The bilayered cellular organization of a Hydra polyp. Ectoderm and endoderm are separated by an acellular matrix called the mesogloea (gray). All epithelial cells in Hydra are myoepithelial, with myofibers on the basal side (red). In ectodermal epithelial cells (green), the fibers are oriented longitudinally, and in endodermal epithelial cells (pink) they are oriented circumferentially (ring muscle). Most interstitial cells and nematoblast clusters are located between ectodermal epithelial cells. Neurons are found in both the endoderm and ectoderm. Sensory neurons are located between epithelial cells and connect to ganglion neurons (purple), which are at the base of the epithelium on top of the myofibers and sometimes cross the mesogloea. Different types of gland cells, most of which are found in the endoderm, are intermingled between the epithelial cells.
Fig. 5.
Fig. 5.
Transgenic cnidarians. (A,B) A transgenic colony of the marine hydrozoan Hydractinia echinata, driving enhanced green fluorescent protein (eGFP, green) under the control of an actin promoter (act::GFP) in all cells. Dark-field (A) and fluorescent (B) images are shown. (C-E) Transgenic Hydra, with the oral end up. (C) A somatic patch of transgenic ectodermal epithelial cells expressing eGFP under the control of an actin promoter, demonstrating normal axial tissue displacement with growth. (D) Somatic first generation transgenic line expressing act::GFP only in the interstitial cell lineage and its derivatives as a result of late integration after segregation of the stem cell lineage. (E) Transgenic Hydra expressing an actin promoter-driven DsRed2 transgene (act::dsRed, red) in the ectoderm. (F-H) Transgenic Nematostella. (F) Transgenic F1 primary polyp expressing mCherry (red) under the control of a muscle-specific promoter (MyHC::mCherry). (G) Cryo-cross section through the mesentery of an adult polyp showing retractor muscle-specific transgene expression (red) and nuclei staining (DAPI, blue). (H) Confocal longitudinal section of a mesentery of a double-transgenic line expressing a neuron-specific transgene (neuract::GFP, green) and a marker of transgenic retractor muscles (MyHC::mCherry, red) showing close association (merge in yellow) of neurons with muscle cells. Images courtesy of Günter Plickert (A,B), Thomas C. Bosch (C,D), Catherine Dana and R.E.S. (E) and E. Renfer and U.T. (G,H). Image in F reproduced with permission (Renfer et al., 2010). Scale bars: 2 mm in A; 500 μm in C-E; 200 μm in F; 250 μm in G; 100 μm in H.
Fig. 6.
Fig. 6.
Symmetry break and asymmetric expression of BMP-like genes and BMP antagonists in Nematostella embryos. (A,B) Early gastrula stage (oral view) showing radial expression of a BMP antagonist, the Nematostella homolog chordin (chd, A), and of the Nematostella BMP2 homolog dpp (B). (C) Double in situ hybridization of chordin and dpp showing that during the mid-gastrula stage, a symmetry break occurs and both genes become expressed on the same side of the blastopore. (D,E) During the planula stage, expression of chordin remains lateral to the blastopore (D), whereas dpp is largely expressed in an endodermal stripe and in a spot at the border of the blastopore (E), on the side of chordin expression. (F) Double in situ hybridization of chordin and dpp in a planula larva showing that both genes remain expressed asymmetrically, on the same side, but segregate with respect to ectoderm and endoderm. Asterisks mark the blastopore. Scale bar: 100 μm. (G) Schematic of the planula stage illustrating the asymmetric expression of chordin and dpp on one side, and of gdf5-like, a member of the BMP family, and of gremlin, a BMP antagonist, on the opposite side. Note that a number of other genes (not shown for clarity) are also expressed asymmetrically, indicative of a directive axis. (H) Double negative-feedback loop between Dpp and Chordin as suggested by morpholino-mediated gene knockdown experiments (Saina et al., 2009). Images in A-G are reproduced with permission (Rentzsch et al., 2006).

Similar articles

See all similar articles

Cited by 61 PubMed Central articles

See all "Cited by" articles

Publication types

LinkOut - more resources

Feedback