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

Dev Biol. 2017 Nov 1;431(1):48-58. doi: 10.1016/j.ydbio.2017.08.017. Epub 2017 Aug 15.

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.

Keywords: Ampullary organs; Electroreceptors; Fgf signaling; Hair cells; Neuromasts; Notch signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Fibroblast Growth Factors / genetics
  • Fibroblast Growth Factors / metabolism*
  • Fish Proteins / genetics
  • Fish Proteins / metabolism*
  • Fishes / genetics
  • Fishes / growth & development*
  • Fishes / metabolism*
  • Gene Expression Regulation, Developmental
  • In Situ Hybridization
  • Lateral Line System / growth & development*
  • Lateral Line System / metabolism*
  • Mechanoreceptors / metabolism*
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism*
  • Sense Organs / growth & development
  • Sense Organs / innervation
  • Sense Organs / metabolism
  • Sensory Receptor Cells / metabolism
  • Signal Transduction
  • Zebrafish / genetics
  • Zebrafish / growth & development
  • Zebrafish / metabolism
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism

Substances

  • Fish Proteins
  • Receptors, Notch
  • Zebrafish Proteins
  • Fibroblast Growth Factors