The freshwater cnidarian Hydra was first described in 17021 and has been the object of study for 300 years. Experimental studies of Hydra between 1736 and 1744 culminated in the discovery of asexual reproduction of an animal by budding, the first description of regeneration in an animal, and successful transplantation of tissue between animals2. Today, Hydra is an important model for studies of axial patterning3, stem cell biology4 and regeneration5. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis6 and other animals. The Hydra genome has been shaped by bursts of transposable element expansion, horizontal gene transfer, trans-splicing, and simplification of gene structure and gene content that parallel simplification of the Hydra life cycle. We also report the sequence of the genome of a novel bacterium stably associated with H. magnipapillata. Comparisons of the Hydra genome to the genomes of other animals shed light on the evolution of epithelia, contractile tissues, developmentally regulated transcription factors, the Spemann–Mangold organizer, pluripotency genes and the neuromuscular junction.
Elucidation of macroevolutionary transitions between diverse animal body plans remains a major challenge in evolutionary biology. We address the sponge-eumetazoan transition by analyzing expression of a broad range of eumetazoan developmental regulatory genes in Sycon ciliatum (Calcispongiae). Here we show that many members of surprisingly numerous Wnt and Tgfb gene families are expressed higher or uniquely in the adult apical end and the larval posterior end. Genes involved in formation of the eumetazoan endomesoderm, such as b-catenin, Brachyury and Gata, as well as germline markers Vasa and Pl10, are expressed during formation and maintenance of choanoderm, the feeding epithelium of sponges. Similarity in developmental gene expression between sponges and eumetazoans, especially cnidarians, is consistent with Haeckel's view that body plans of sponges and cnidarians are homologous. These results provide a framework for further studies aimed at deciphering ancestral developmental regulatory networks and their modifications during animal body plans evolution.
The dickkopf (dkk) gene family encodes secreted antagonists of Wnt signalling proteins, which have important functions in the control of cell fate, proliferation, and cell polarity during development. Here, we report the isolation, from a regeneration-specific signal peptide screen, of a novel dickkopf gene from the fresh water cnidarian Hydra. Comparative sequence analysis demonstrates that the Wnt antagonistic subfamily Dkk1/Dkk2/Dkk4 and the non-modulating subfamily Dkk3 separated prior to the divergence of cnidarians and bilaterians. In steady-state Hydra, hydkk1/2/4-expression is inversely related to that of hywnt3a. hydkk1/2/4 is an early injury and regeneration responsive gene, and hydkk1/2/4-expressing gland cells are essential for head regeneration in Hydra, although once the head has regenerated they are excluded from it. Activation of Wnt/-Catenin signalling leads to the complete downregulation of hydkk1/2/4 transcripts. When overexpressed in Xenopus, HyDkk1/2/4 has similar Wnt-antagonizing activity to the Xenopus gene Dkk1. Based on the corresponding expression patterns of hydkk1/2/4 and neuronal genes, we suggest that the body column of Hydra is a neurogenic environment suppressing Wnt signalling and facilitating neurogenesis.
Cnidarians are the simplest metazoans with a nervous system. They are well known for their regeneration capacity, which is based on the restoration of a signalling centre (organizer). Recent work has identified the canonical Wnt pathway in the freshwater polyp Hydra, where it acts in organizer formation and regeneration. Wnt signalling is also essential for cnidarian embryogenesis. In the sea anemone Nematostella vectensis 11 of the 12 known wnt gene subfamilies were identified. Different wnt genes exhibit serial and overlapping expression domains along the oral-aboral axis of the embryo (the 'wnt code'). This is reminiscent of the hox code (cluster) in bilaterian embryogenesis that is, however, absent in cnidarians. It is proposed that the common ancestor of cnidarians and bilaterians invented a set of wnt genes that patterned the ancient main body axis. Major antagonists of Wnt ligands (e.g. Dkk 1/2/4) that were previously known only from chordates, are also present in cnidarians and exhibit a similar conserved function. The unexpectedly high level of genetic complexity of wnt genes evolved in early multi-cellular animals about 650 Myr ago and suggests a radical expansion of the genetic repertoire, concurrent with the evolution of multi-cellularity and the diversification of eumetazoan body plans. Oncogene (2006Oncogene ( ) 25, 7450-7460. doi:10.1038 Keywords: Wnt signalling; regeneration; axis formation; Hydra; Nematostella; cnidaria Cnidarians are genetically complexThe Cnidaria is an ancient metazoan phylum of diploblastic animals including freshwater polyps and hydroids, sea anemones and corals, and jellyfish. All cnidarians share the same simple body plan that is reminiscent of an early bilaterian gastrula. However, they are lacking the mesoderm and possess only two germ layers, an outer ectoderm and inner endoderm that are separated by an acellular mesogloea. Cnidaria are a sister-group to the Bilateria (Figure 1), and the fossil record reveals that cnidarians are >500 Myr old (Chen et al., 2000(Chen et al., , 2002Conway Morris, 2000). They are of crucial importance for unravelling the origin and evolution of major signalling pathways in animal evolution.There are two major genetic model systems for cnidarians: the well-known freshwater polyp Hydra (Steele, 2006) and the starlet sea anemone Nematostella vectensis (Holland, 2004;Darling et al., 2005), which was introduced by the pioneering work of Cadet Hand (Hand and Uhlinger, 1992). Recent EST projects in these and some other cnidarian taxa have revealed an astonishing and unexpected genetic complexity of cnidarians. Analyses of ESTs from the anthozoans Acropora millepora and Nematostella vectensis have lead to the identification of 16 571 non-redundant ESTs and 12 547 predicted peptides across the two species (7484 from Nematostella and 5063 from Acropora (Miller et al., 2005;Technau et al., 2005). Both data sets are far from saturation and one can estimate that anthozoan genomes are likely to contain 25 000 genes, which is in the same range as vertebr...
BackgroundSox genes are HMG-domain containing transcription factors with important roles in developmental processes in animals; many of them appear to have conserved functions among eumetazoans. Demosponges have fewer Sox genes than eumetazoans, but their roles remain unclear. The aim of this study is to gain insight into the early evolutionary history of the Sox gene family by identification and expression analysis of Sox genes in the calcareous sponge Sycon ciliatum.MethodsCalcaronean Sox related sequences were retrieved by searching recently generated genomic and transcriptome sequence resources and analyzed using variety of phylogenetic methods and identification of conserved motifs. Expression was studied by whole mount in situ hybridization.ResultsWe have identified seven Sox genes and four Sox-related genes in the complete genome of Sycon ciliatum. Phylogenetic and conserved motif analyses showed that five of Sycon Sox genes represent groups B, C, E, and F present in cnidarians and bilaterians. Two additional genes are classified as Sox genes but cannot be assigned to specific subfamilies, and four genes are more similar to Sox genes than to other HMG-containing genes. Thus, the repertoire of Sox genes is larger in this representative of calcareous sponges than in the demosponge Amphimedon queenslandica. It remains unclear whether this is due to the expansion of the gene family in Sycon or a secondary reduction in the Amphimedon genome. In situ hybridization of Sycon Sox genes revealed a variety of expression patterns during embryogenesis and in specific cell types of adult sponges.ConclusionsIn this study, we describe a large family of Sox genes in Sycon ciliatum with dynamic expression patterns, indicating that Sox genes are regulators in development and cell type determination in sponges, as observed in higher animals. The revealed differences between demosponge and calcisponge Sox genes repertoire highlight the need to utilize models representing different sponge lineages to describe sponge development, a prerequisite for deciphering evolution of metazoan developmental mechanisms.
Signaling centers or organizers play a key role in axial patterning processes in animal embryogenesis. The function of most vertebrate organizers involves the activity of secreted antagonists of bone morphogenetic proteins (BMPs) such as Chordin or Noggin. Although BMP homologs have been isolated from many phyla, the evolutionary origin of the antagonistic BMP/Chordin system in organizer signaling is presently unknown. Here we describe a Chordin-like molecule (HyChdl) from Hydra that inhibits BMP activity in zebrafish embryos and acts in Hydra axis formation when new head organizers are formed during budding and regeneration. hychdl transcripts are also up-regulated in the head regeneration-deficient mutant strain reg-16. Accordingly, HyChdl has a function in organizer formation, but not in head differentiation. Our data indicate that the BMP/Chordin antagonism is a basic property of metazoan signaling centers that was invented in early metazoan evolution to set up axial polarity.axis formation ͉ bone morphogenetic protein/Chordin ͉ Cnidaria ͉ regeneration ͉ signaling L ocalized signaling centers or organizers are widely used for the patterning of embryos or tissues during animal development. In general, organizers are able to generate polarity in surrounding tissue and to induce specific cell fates and cell behavior (1). One of the best-characterized examples is the amphibian embryonic organizer known as the Spemann-Mangold organizer (2). This organizer, localized at the dorsal blastopore lip, is able to induce the formation of a second body axis upon transplantation to the ventral side of a host embryo. The inductive capacity of the organizer is demonstrated by its ability to recruit host tissue into the second axis (3, 4). Functionally equivalent embryonic organizers are found in most vertebrates, including the node in amniotes and the embryonic shield in teleosts (5). The evolutionary origin of the embryonic organizer is unclear at present, but it was proposed that it is a vertebrate-specific invention (6).There is evidence that the embryonic organizer is much older than commonly assumed. In the freshwater polyp Hydra, a member of the Ͼ500-million-year-old phylum Cnidaria, Browne (7) demonstrated the existence of an organizer-like activity already in 1909: Transplantation of a hypostome into the body column of a labeled host led to the formation of a second body axis including hostderived tissue (7,8). The hypostome is the oral end of a cnidarian body axis and corresponds to the blastopore of a gastrula. However, whether the head organizer of Hydra represents the evolutionary origin of the vertebrate embryonic organizer or whether they arose independently is currently not known.On the molecular level, Wnt/-catenin signaling and the inhibition of bone morphogenetic protein (BMP) signaling by secreted antagonist such as Chordin and Noggin play a pivotal role in the establishment of the Spemann-Mangold organizer in Xenopus and the shield in zebrafish (4, 9, 10) as well as in the establishment of axial polarity...
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