Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

Abstract

Cnidarians represent the first animal phylum with an organized nervous system and a complex active behavior. The hydra nervous system is formed of sensory-motoneurons, ganglia neurons and mechanoreceptor cells named nematocytes, which all differentiate from a common stem cell. The neurons are organized as a nerve net and a subset of neurons participate in a more complex structure, the nerve ring that was identified in most cnidarian species at the base of the tentacles. In order to better understand the genetic control of this neuronal network, we analysed the expression of evolutionarily-conserved regulatory genes in the hydra nervous system. The PRD-CLASS homeogene, prdl-b, and the nuclear orphan receptor, hyCOUP-TF, are expressed at strong levels in proliferating nematoblasts, a lineage where they were found repressed during patterning and morphogenesis, and at low levels in distinct subsets of neurons. Interestingly, PRD-CLASS homeobox and COUP-TF genes are also expressed during neurogenesis in bilaterians, suggesting that mechanoreceptor and neuronal cells derive from a common ancestral cell. Moreover, the PRD-CLASS homeobox gene prdl-a, the ANTP-CLASS homeobox gene msh, and the thrombospondin-related gene TSP1, which are expressed in distinct subset of neurons in the adult polyp, are also expressed during early budding and/or head regeneration. These data strengthen the fact that two distinct regulations, one for neurogenesis and another for patterning, already apply to these regulatory genes, a feature also identified in bilaterian related-genes.

Molecular evidence for deep evolutionary roots of bilaterality in animal development

“…Immunohistochemical studies have shown a great deal of molecular complexity in neuropeptide expression in Hydra (66,67), and gene expression studies with an increasingly broad range of molecular markers with potential roles in neural patterning have highlighted distinct domains of the N. vectensis body plan. NvNetrin is expressed in the same longitudinal stripe of body wall where several Hox genes are expressed.…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Notably, signalling through the RXR receptor has been examined in several species of cnidarian; exogenous application of retinoic acid has been shown to play a role in promoting metamorphosis in the jellyfish Aurelia aurita [94] and regulating the development of the eyes in the box jelly Tripedalia cystophora [95]. Further, the COUP-TF transcription factor (NR2 family) is an important regulator of neurogenesis in hydrozoans [96,97]. While Reitzel & Tarrant [87] demonstrated differential expression of NRs through developmental time in N. vectensis, without spatial analysis of gene expression it is difficult to hypothesize what role these diverse receptors may play in embryogenesis of the sea anemone.…”

Neuroglobins, Pivotal Proteins Associated with Emerging Neural Systems and Precursors of Metazoan Globin Diversity

“…Together with the ctenophores, the Cnidaria form the Coelenterata, the sister group of Bilateria (52). It is assumed that transduction of chemical and mechanical stimuli in nematocytes are hallmarks of primitive nerve cells and that nematocytes are thus representative of ancestral sensory cells that preceded the differentiation of neuronal cell types in animal evolution (53). The unequivocal expression of Ngbs in nematocytes of the jellyfish C. hemisphaerica appears to be a robust indication of the essential role of these proteins in early evolution of the nervous system.…”