ReviewConserved and divergent genes in apex and axis development of cnidarians
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
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References (65)
- et al.
Appearance and disappearance of Syk family protein-tyrosine kinase genes during metazoan evolution
Gene
(1999) - et al.
Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea
Mech Dev
(2000) Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation
Dev Biol
(1983)- et al.
Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra
Dev Biol
(1997) - et al.
CnOtx, a member of the Otx gene family, has a role in cell movement in hydra
Dev Biol
(1999) - et al.
The homeobox gene Otx of the jellyfish Podocoryne carnea: role of a head gene in striated muscle and evolution
Dev Biol
(1999) - et al.
Arachidonic acid, protein kinase C activators and bud formation in Hydra vulgaris
Comp Biochem Physiol
(1993) - et al.
Origin of anterior patterning. How old is our head?
Trends Genet
(2000) - et al.
Transdifferentiation occurs continuously in a adult hydra
Curr Top Dev Biol
(1986) - et al.
CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra
Dev Biol
(1996)
Expression of a novel receptor tyrosine kinase gene and a paired-like homeobox gene provides evidence of differences in patterning at the oral and aboral ends of hydra
Dev Biol
Hydra metalloproteinase 1: a secreted astacin metalloproteinase whose apical axis expression is differentially regulated during head regeneration
Dev Biol
Colinearity and functional hierarchy among genes of the homeotic complexes
Trends Genet
Homology of hox genes and the zootype concept in early metazoan evolution
Mol Phylogenet Evol
The evolution of ‘bricolage’
Trends Genet
Silencing of developmental genes in Hydra
Dev Biol
Expression and developmental regulation of the Hydra-RFamide and Hydra-LWamide preprohormone genes in Hydra: evidence for transient phases of head formation
Dev Biol
Isolation of a marker for head-specific cell differentiation in hydra
Differentiation
The zootype and the phylotypic stage
Nature
The coral Acropora: what it can contribute to our knowledge of metazoan evolution and the evolution of developmental processes
Bioessays
Regeneration of hydra from reaggregated cells
Nat New Biol
Hydrozoa metamorphosis and pattern formation
Curr Top Dev Biol
Identification of caspases and apoptosis in the simple metazoan Hydra
Curr Biol
Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning
Proc Natl Acad Sci USA
Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): implications for the evolution of the Pax gene family
Proc Natl Acad Sci USA
The cAMP response element binding protein is involved in hydra regeneration
Development
prdl-a, a gene marker for hydra apical differentiation related to triploblastic paired-like head-specific genes
Development
Retinoic acid X receptor in the diploblast, Tripedalia cystophora
Proc Natl Acad Sci USA
Genomic organization of a voltage-gated Na+ channel in a hydrozoan jellyfish: insights into the evolution of voltage-gated Na+ channel genes
Recept Channels
The production of new hydranths in hydra by the insertion of small grafts
J Exp Zool
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