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.
Members of the Wnt/wingless family of secreted proteins act as short-range inducers and long-range organizers during axis formation, organogenesis and tumorigenesis in many developing tissues. Wnt signalling pathways are conserved in nematodes, insects and vertebrates. Despite its developmental significance, the evolutionary origin of Wnt signalling is unclear. Here we describe the molecular characterization of members of the Wnt signalling pathway--Wnt, Dishevelled, GSK3, beta-Catenin and Tcf/Lef--in Hydra, a member of the evolutionarily old metazoan phylum Cnidaria. Wnt and Tcf are expressed in the putative Hydra head organizer, the upper part of the hypostome. Wnt, beta-Catenin and Tcf are transcriptionally upregulated when head organizers are established early in bud formation and head regeneration. Wnt and Tcf expression domains also define head organizers created by de novo pattern formation in aggregates. Our results indicate that Wnt signalling may be involved in axis formation in Hydra and support the idea that it was central in the evolution of axial differentiation in early multicellular animals.
The Wnt gene family encodes secreted signalling molecules that control cell fate in animal development and human diseases. Despite its significance, the evolution of this metazoan-specific protein family is unclear. In vertebrates, twelve Wnt subfamilies were defined, of which only six have counterparts in Ecdysozoa (for example, Drosophila and Caenorhabditis). Here, we report the isolation of twelve Wnt genes from the sea anemone Nematostella vectensis, a species representing the basal group within cnidarians. Cnidarians are diploblastic animals and the sister-group to bilaterian metazoans. Phylogenetic analyses of N. vectensis Wnt genes reveal a thus far unpredicted ancestral diversity within the Wnt family. Cnidarians and bilaterians have at least eleven of the twelve known Wnt gene subfamilies in common; five subfamilies appear to be lost in the protostome lineage. Expression patterns of Wnt genes during N. vectensis embryogenesis indicate distinct roles of Wnts in gastrulation, resulting in serial overlapping expression domains along the primary axis of the planula larva. This unexpectedly complex inventory of Wnt family signalling factors evolved in early multi-cellular animals about 650 million years (Myr) ago, predating the Cambrian explosion by at least 100 Myr (refs 5, 8). It emphasizes the crucial function of Wnt genes in the diversification of eumetazoan body plans.
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.
In and evaginations of 2D cell sheets are major shape generating processes in animal development. They result from directed movement and intercalation of polarized cells associated with cell shape changes. Work on several bilaterian model organisms has emphasized the role of noncanonical Wnt signaling in cell polarization and movement. However, the molecular processes responsible for generating tissue and body shape in ancestral, prebilaterian animals are unknown. We show that noncanonical Wnt signaling acts in mass tissue movements during bud and tentacle evagination and regeneration in the cnidarian polyp Hydra. The wnt5, wnt8, frizzled2 ( fz2), and dishevelled-expressing cell clusters define the positions, where bud and tentacle evaginations are initiated; wnt8, fz2, and dishevelled remain up-regulated in those epithelial cells, undergoing cell shape changes during the entire evagination process. Downstream of wnt and dsh expression, JNK activity is required for the evagination process. Multiple ectopic wnt5, wnt8, fz2, and dishevelled-expressing centers and the subsequent evagination of ectopic tentacles are induced throughout the body column by activation of Wnt/-Catenin signaling. Our results indicate that integration of axial patterning and tissue morphogenesis by the coordinated action of canonical and noncanonical Wnt pathways was crucial for the evolution of eumetazoan body plans.cnidaria ͉ convergent extension ͉ morphogenesis ͉ actin ͉ JNK
The c-myc protooncogene encodes a transcription factor (Myc) with oncogenic potential. Myc and its dimerization partner Max are bHLH-Zip DNA binding proteins controlling fundamental cellular processes. Deregulation of c-myc leads to tumorigenesis and is a hallmark of many human cancers. We have identified and extensively characterized ancestral forms of myc and max genes from the early diploblastic cnidarian Hydra, the most primitive metazoan organism employed so far for the structural, functional, and evolutionary analysis of these genes. Hydra myc is specifically activated in all stem cells and nematoblast nests which represent the rapidly proliferating cell types of the interstitial stem cell system and in proliferating gland cells. In terminally differentiated nerve cells, nematocytes, or epithelial cells, myc expression is not detectable by in situ hybridization. Hydra max exhibits a similar expression pattern in interstitial cell clusters. The ancestral Hydra Myc and Max proteins display the principal design of their vertebrate derivatives, with the highest degree of sequence identities confined to the bHLH-Zip domains. Furthermore, the 314-amino acid Hydra Myc protein contains basic forms of the essential Myc boxes I through III. A recombinant Hydra Myc/Max complex binds to the consensus DNA sequence CACGTG with high affinity. Hybrid proteins composed of segments from the retroviral v-Myc oncoprotein and the Hydra Myc protein display oncogenic potential in cell transformation assays. Our results suggest that the principal functions of the Myc master regulator arose very early in metazoan evolution, allowing their dissection in a simple model organism showing regenerative ability but no senescence.cell proliferation | cnidaria | development | transcription factor
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...
Self-organization has been demonstrated in a variety of systems ranging from chemical-molecular to ecosystem levels, and evidence is accumulating that it is also fundamental for animal development. Yet, self-organization can be approached experimentally in only a few animal systems. Cells isolated from the simple metazoan Hydra can aggregate and form a complete animal by self-organization. By using this experimental system, we found that clusters of 5-15 epithelial cells are necessary and sufficient to form de novo head-organizing centers in an aggregate. Such organizers presumably arise by a community effect from a small number of cells that express the conserved HyBra1 and HyWnt genes. These local sources then act to pattern and instruct the surrounding cells as well as generate a field of lateral inhibition that ranges up to 1,000 m. We propose that conserved patterning systems in higher animals originate from extremely robust and flexible molecular self-organizing systems that were selected for during early metazoan evolution.A nimal development is commonly explained in terms of hierarchical genetic cascades that begin with an initial asymmetry based on either maternal or external cues. In Drosophila, for instance, complex cellular interactions during oogenesis eventually lead to the local deposition of maternal messages in the oocyte that determine the body axes (1, 2). In the Xenopus embryo, a pre-established animal-vegetal asymmetry in the egg and sperm entry point determine the location of the anterior-posterior and the dorsoventral axes by locally initiating genetic cascades that lead to the formation of the future organizer (3, 4). Less clear is how an organizer is set up in tissue without inherent asymmetry or external cues.Only a few animal systems are amenable to the experimental analysis of self-organization during development (5-7). The simple metazoan Hydra is particularly useful in this context, because its body plan and any positional information can be completely destroyed and re-established in dissociationreaggregation studies. Hydra consists of a single axis with a head and foot at either end of a tubular body column. The axial pattern of the animal is maintained by a gradient of head formation competence, commonly referred to as the head activation gradient (8), or source density gradient (9). The term gradient of head formation competence, or more simply gradient of head competence, is in line with current terminology and will be used in this work. (The term head activation will be used for the actual process of head formation.) This head competence gradient reflects the ability of tissue of the body column to form a head either on bisection leading to head regeneration at the apical end of the lower half, or on transplantation of a piece of the body column to the body column of a second animal. The gradient is maximal near the head decreasing down the body column and is a relatively stable property of the body column (8). Head formation in the body column is prevented by a head inhibition...
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