Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish

Abstract

The lateral line system is a useful model for studying the embryonic and evolutionary diversification of different organs and cell types. In jawed vertebrates, this ancestrally comprises lines of mechanosensory neuromasts over the head and trunk, flanked on the head by fields of electrosensory ampullary organs, all innervated by lateral line neurons in cranial lateral line ganglia. Both types of sense organs, and their afferent neurons, develop from cranial lateral line placodes. Current research primarily focuses on the posterior lateral line primordium in zebrafish, which migrates as a cell collective along the trunk; epithelial rosettes form in the trailing zone and are deposited as a line of neuromasts, within which hair cells and supporting cells differentiate. However, in at least some other teleosts (e.g. catfishes) and all non-teleosts, lines of cranial neuromasts are formed by placodes that elongate to form a sensory ridge, which subsequently fragments, with neuromasts differentiating in a line along the crest of the ridge. Furthermore, in many non-teleost species, electrosensory ampullary organs develop from the flanks of the sensory ridge. It is unknown to what extent the molecular mechanisms underlying neuromast formation from the zebrafish migrating posterior lateral line primordium are conserved with the as-yet unexplored molecular mechanisms underlying neuromast and ampullary organ formation from elongating lateral line placodes. Here, we report experiments in an electroreceptive non-teleost ray-finned fish, the Mississippi paddlefish Polyodon spathula, that suggest a conserved role for Notch signaling in regulating lateral line organ receptor cell number, but potentially divergent roles for the fibroblast growth factor signaling pathway, both between neuromasts and ampullary organs, and between paddlefish and zebrafish.

Transcriptome profiles of sturgeon lateral line electroreceptor and mechanoreceptor during regeneration

“…potassium channels are used for rapid vesicular release from elaborate ribbon synapses, which is adaptive for predation [24,25]. Recent years, Backer et al reported several works on AOs and NMs gene expression for paddlefish [16][17][18]26], which is relative close to sturgeon phylogenetically. We found many consistencies between our study and theirs.…”

“…Molecular mechanisms for these differences are not clearly understood. Several studies, including analyses of the sensory epithelium transcriptome of paddlefish, have identified some genes commonly expressed in both AOs and NMs, including notch1, atoh1, eya1, eya4, parvalbumin-3, pou4f3 and so on [16][17][18]. However, the systemic transcriptome comparison between AOs and NMs was seldom reported.…”

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

“…Three originally unassigned loci in the paddlefish lateral line organ-enriched dataset (Modrell et al, 2017a), all of whose closest UniProt matches had Pfam Hairy Orange and helix-loop-helix DNA-binding domains (locus 52662, 2.7-fold lateral line-enriched; locus 27975, 2.9-fold lateral line-enriched; locus 26264, 2.3-fold lateral line-enriched), proved to represent the related Notch target and effector gene Hes5. We had previously published the expression of Hes5 in both ampullary organs and neuromasts in a study on the role of Notch signalling in ampullary organ versus neuromast development in paddlefish (Modrell et al, 2017b) Expression in developing ampullary organs and neuromasts was also seen for Tfap2d (Figure 3O,P; 6.0-fold lateral line-enriched, Modrell et al, 2017a). This gene encodes transcription factor AP-2 delta, which is a direct activator of Pou4f3 in retinal ganglion cell progenitors (Hesse et al, 2011;Li et al, 2016).…”

Identification, Characterization and Functional Analysis of Fibroblast Growth Factors in Black Rockfish (Sebastes schlegelii)

“…In fishes, FGFs have also been widely identified to be involved in multiple biological processes. For example, Fgf signaling has been shown to participate in electrosensory versus mechanosensory lateral line organ development in non-teleost ray-finned fish [ 20 ]. In stickleback, the expression profiles of FGF8a and FGF8b during embryo development suggest their functional divergence.…”