The dynamic genome of Hydra.

The freshwater cnidarian Hydra was first described in 1702 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 animals. Today, Hydra is an important model for studies of axial patterning, stem cell biology and regeneration. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis 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.

Multiple Wnts are involved in Hydra organizer formation and regeneration.

Wnt genes and beta-catenin signaling are involved in axial patterning processes in vertebrate embryogenesis in setting up the Spemann-Mangold organizer in amphibian embryos. An organizer with a similar function is present in the hypostome of an adult Hydra polyp. Previously, a Hydra ortholog of Wnt3 (HyWnt3), which is expressed in the hypostome, has been described. Here, ten additional Hydra Wnt genes have been identified. Of these, six (HyWnt1, -7, -9/10a, -9/10c, -11, and -16) are expressed in the adult hypostome. And, as is HyWnt3, these six Wnt genes are also expressed when a new head organizer is formed during head regeneration and bud formation. The kinetics of Wnt gene expressions during head regeneration suggests that a cascade of consecutive Wnt activation accompanies regeneration, and HyWnt3 begins this cascade. Recombinant HyWnt3 protein induced body column tissue to undergo head formation. It also increased the head formation capacity in the head regeneration-deficient mutant strain reg-16 to that of wild-type strains. In addition our data reveal striking similarities in the molecular basis of the organizer in Hydra and axis polarization in chordates (e.g. Spemann's organizer) as well as it's role in regeneration suggesting a conserved function of Wnt signaling in setting up this ancient metazoan signaling center.

Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes.

Cnidaria are the first class of organisms in animal evolution with a nervous system. The cnidarian Hydra has two types of neuronal cell, nerve cells and nematocytes. Both differentiate from the same pool of pluripotent stem cells. Yet, the molecular regulation of neural differentiation in Hydra is largely unknown. Here, we report the identification of Hyzic, a homolog of the Zn-finger transcription factor gene zic/odd-paired, which acts as an early neural effector gene in vertebrates. We show, that Hyzic is expressed in the early nematocyte differentiation pathway, starting at the level of interstitial stem cells. Expression of Hyzic is restricted to the proliferative stages of nematoblasts. Hyzic acts before and possibly directly upstream of Cnash, a homolog of the proneural bHLH transcription factor gene achaete-scute, and of Nowa, an early nematocyte differentiation marker gene. Hyzic may determine stem cells to differentiate into nematocytes. Our data are consistent with a role of Hyzic in inhibiting nematocyte differentiation, by keeping committed nematoblast cells in the cell cycle. A similar role has been demonstrated for Zic genes in vertebrates. Our results suggest, that genetic cascades of neural development may be conserved from Hydra to vertebrates, indicating that the molecular regulation of neural development evolved only once.