A genomic view of the sea urchin nervous system

Abstract

The sequencing of the Strongylocentrotus purpuratus genome provides a unique opportunity to investigate the function and evolution of neural genes. The neurobiology of sea urchins is of particular interest because they have a close phylogenetic relationship with chordates, yet a distinctive pentaradiate body plan and unusual neural organization. Orthologues of transcription factors that regulate neurogenesis in other animals have been identified and several are expressed in neurogenic domains before gastrulation indicating that they may operate near the top of a conserved neural gene regulatory network. A family of genes encoding voltage-gated ion channels is present but, surprisingly, genes encoding gap junction proteins (connexins and pannexins) appear to be absent. Genes required for synapse formation and function have been identified and genes for synthesis and transport of neurotransmitters are present. There is a large family of G-protein-coupled receptors, including 874 rhodopsin-type receptors, 28 metabotropic glutamate-like receptors and a remarkably expanded group of 161 secretin receptor-like proteins. Absence of cannabinoid, lysophospholipid and melanocortin receptors indicates that this group may be unique to chordates. There are at least 37 putative G-protein-coupled peptide receptors and precursors for several neuropeptides and peptide hormones have been identified, including SALMFamides, NGFFFamide, a vasotocin-like peptide, glycoprotein hormones and insulin/insulin-like growth factors. Identification of a neurotrophin-like gene and Trk receptor in sea urchin indicates that this neural signaling system is not unique to chordates. Several hundred chemoreceptor genes have been predicted using several approaches, a number similar to that for other animals. Intriguingly, genes encoding homologues of rhodopsin, Pax6 and several other key mammalian retinal transcription factors are expressed in tube feet, suggesting tube feet function as photosensory organs. Analysis of the sea urchin genome presents a unique perspective on the evolutionary history of deuterostome nervous systems and reveals new approaches to investigate the development and neurobiology of sea urchins.

Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6

“…Note the presence of the pigment cells, probably containing opsin, in and around the ossicles (figure 2g). Nerves are also present along the entire length of the tube foot under the epithelium, forming a nerve plexus (figure 2h) that terminates in a ganglion at the distal portion of the tube foot as previously described for sea urchins [30][31][32]. Using primers specific for opsins, a 1.563 Kbp cDNA was amplified from the green sea urchin tube foot.…”

“…First described in Xenopus, melanopsin is now known to confer photosensitivity on non-photosensitive cells types [50,51]. It has been hypothesized that melanopsin sets the circadian clock through non-ocular light detection [52], and is also expressed in sea urchins [30]. Additionally, an encephalopsin homologue has been sequenced from sea urchins [30,41], which is expressed at the tips of the larval arms of plutei and tube feet of adults [16,41], and potentially aids in the detection of light by planktonic larvae vertically migrating in the water column.…”

“…In response to changes in the underwater light field, the light absorbed by the opsins of the pigment cells could potentially stimulate the nerves beneath them and conduct electrical information along the major nerve that passes along one side of each tube foot towards the test of the urchin. We now know that a full array of genes encoding neurotransmitters is present in sea urchins, which could facilitate the transmission of these signals [30]. For temperate invertebrates like the green sea urchin, opsins are well suited to mediate this transduction of an external environmental signal because of their absorption maxima in the bluegreen portion of the spectrum that dominates in these underwater habitats [3,54].…”

Unique system of photoreceptors in sea urchin tube feet

“…Moreover, six different opsins plus other essential components of the signal transduction cascade of photoreceptor cells (PRCs) were identified (10,11). RT-PCR showed that many of the discovered genes are expressed in adult S. purpuratus tube feet (10,11), suggesting the presence of a more elaborate light-sensing apparatus than was previously assumed.…”

“…The genome sequencing of the purple sea urchin Strongylocentrotus purpuratus led to the surprising discovery of a large number of typical "eye" genes, like pax6, atonal, neuroD, and barh1, which in vertebrates pattern early retina development (10). Moreover, six different opsins plus other essential components of the signal transduction cascade of photoreceptor cells (PRCs) were identified (10,11).…”