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Elife. 2017 Mar 27;6. pii: e24197. doi: 10.7554/eLife.24197.

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

Author information

1
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.
2
Cambridge Systems Biology Centre, University of Cambridge, Cambridge, United Kingdom.
3
Department of Genetics, University of Cambridge, Cambridge, United Kingdom.
4
Department of Neuroscience, The University of Texas at Austin, Austin, United States.
5
Department of Integrative Biology, The University of Texas at Austin, Austin, United States.
6
Departmento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales-MNCN-CSIC, Madrid, Spain.
7
Department of Natural Sciences, Saint Louis University - Madrid Campus, Madrid, Spain.
8
Department of Molecular and Cellular Biology, Kennesaw State University, Kennesaw, United States.

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.

KEYWORDS:

Atoh1; Cav1.3; Cavβ2; Kv1.5; Kvβ3; Neurod4; Polyodon spathula (Mississippi paddlefish); Pou4f3; Vglut3; ampullary organs; beta-parvalbumins; developmental biology; electroreceptors; hair cells; hh; neuromasts; neuroscience; oncomodulin; otoferlin; stem cells; synaptic ribbons; voltage-gated ion channels

PMID:
28346141
PMCID:
PMC5429088
DOI:
10.7554/eLife.24197
[Indexed for MEDLINE]
Free PMC Article

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