Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome.

Melinda S Modrell,David Buckley,Mike Lyne,Adrian R Carr,Gos Micklem,Harold H Zakon,Alexander S Campbell,Clare Vh Baker,Marcus C Davis

doi:10.7554/elife.24197

Abstract

The anamniote lateral line system, comprising mechanosensory neuromasts and electrosensory ampullary organs, is a useful model for investigating the developmental and evolutionary diversification of different organs and cell types. Zebrafish neuromast development is increasingly well understood, but neither zebrafish nor Xenopus is electroreceptive and our molecular understanding of ampullary organ development is rudimentary. We have used RNA-seq to generate a lateral line-enriched gene-set from late-larval paddlefish (Polyodon spathula). Validation of a subset reveals expression in developing ampullary organs of transcription factor genes critical for hair cell development, and genes essential for glutamate release at hair cell ribbon synapses, suggesting close developmental, physiological and evolutionary links between non-teleost electroreceptors and hair cells. We identify an ampullary organ-specific proneural transcription factor, and candidates for the voltage-sensing L-type Cav channel and rectifying Kv channel predicted from skate (cartilaginous fish) ampullary organ electrophysiology. Overall, our results illuminate ampullary organ development, physiology and evolution.

Highlights

The lateral line system of fishes and aquatic amphibians is a good model for studying the diversification of different organs and cell types, both in development and evolution
For the first time in any vertebrate, we identify genes expressed in ampullary organs but not neuromasts, including a transcription factor, a beta-parvalbumin and voltage-gated potassium channel subunits consistent with predictions from skate ampullary organ electrophysiology
Of the 16 transcription factor genes whose expression we have reported to date in developing paddlefish lateral line organs, all except one (Neurod4) are expressed in ampullary organs as well as neuromasts, including transcription factor genes that are essential for hair cell development, such as Atoh1 and Pou4f3 (Brn3c)

Summary

Introduction

The lateral line system of fishes and aquatic amphibians is a good model for studying the diversification of different organs and cell types, both in development and evolution. In jawed vertebrates, this sensory system ancestrally includes mechanosensory neuromasts and electrosensory ampullary organs (‘ampullae of Lorenzini’), both of which develop - together with their afferent neurons - from individual embryonic lateral line placodes (Northcutt et al, 1995; Modrell et al, 2011a; Gillis et al, 2012). The entire lateral line system was lost in amniotes, with the transition to life on land

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