Review
Conserved and divergent genes in apex and axis development of cnidarians

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Abstract

Despite their radial organization and their sister group position in the life tree, cnidarian species express during morphogenesis a large number of genes that are related to bilaterian developmental genes. Among those, homologs to forkhead, emx, aristaless, goosecoid, brachyury, wnt and nanos genes are regulated during apical patterning in cnidarians, suggesting that key components of early organizer activity were conserved across evolution and recruited for either anterior, axial, or dorso-ventral patterning in bilaterians. In contrast, the expression patterns of the cnidarian Hox-related genes suggest that the apical–basal axis of the cnidarian polyp and the anterior–posterior axis of bilaterians do not differentiate following homologous processes.

Section snippets

Introduction: biological diversity in the cnidarian world

Cnidarians together with ctenophores are the most primitive animals that display nerve-cell differentiation and a morphogenetic differentiation along their axis. However, cnidarians that develop from only two main layers—the ectoderm and the endoderm separated by the mesoglea—do not differentiate organs. As a common phylum-specific signature, all cnidarians employ differentiated nematocytes (stinging cells) in their tentacles. Their early divergence during evolution raises the question of the

Molecular conservation from cnidarians to bilaterians

The past few years have been an active period for cloning evolutionarily-conserved genes from cnidarian species and it is now clear that those genes encode highly conserved functional domains—most likely involved in gene regulation, translational control, signal transduction, apoptosis [7], extracellular signalling, and cell/extracellular matrix interactions (see references in Table 1). Those data prove, first, that most if not all of the gene families do have representatives in cnidarians, and

The head, the bud and the regenerating stump: paradigms for the organizer activity

The induction phenomena in biology was first described in 1909 by Elena Browne [16] who grafted pieces of Hydra tissue onto a host and could induce a complete secondary axis. Later on, it was demonstrated that the regenerating stump (RS) displays similar properties, being the site of an ‘unstable head activation’, here named head organizer activity, that reaches a plateau level ∼10 hours after bisection and remains strictly limited to the regenerating tip [17]. Recently, an increasing number of

The polyp axis: a segmented field?

Although the polyp body shape is rather simple (i.e. a tube; Fig. 2a), its morphology results from permanent, dynamic processes—namely proliferation, differentiation and migration—which take place at distinct locations. A pool of stem cells is constantly renewed in the central part of the body column, whereas cells migrating towards the extremities will progressively differentiate and/or transdifferentiate [34]. Interestingly, several genes show clear restricted domains of expression along the

Phylum-specific developmental mechanisms?

Complete bilaterian genomes have now been fully sequenced and at least two genes expressed during apical patterning in Hydra do not have clear cognate genes in any other species as far as is known (Table 1). Furthermore, peptides are very abundant in cnidarians, currently subjected to a systematic characterization [49]. The neuropeptide head activator that speeds up regeneration processes, possibly through nerve-cell differentiation, is evolutionarily conserved as well as its binding protein,

Conclusions

Evolutionary tinkering is most likely the driving force that led to the development of organisms with different complexities [57]. In this view, the high level of gene conservation strengthens the validity of the cnidarian model systems for studying basic developmental processes shared by eumetazoans. Indeed, the recent data suggest that a complete set of key developmental genes was already present and functional in the common ancestor of cnidarians and bilaterians. According to the expression

Acknowledgements

I thank Bert Hobmayer and Thomas Holstein for communicating data before publication, and Toshi Fujisawa for helpful comments on the manuscript. The work in my laboratory is supported by the Swiss National Foundation and the Canton de Genève.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

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