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

Author:

Modrell Melinda S1,Lyne Mike23,Carr Adrian R23,Zakon Harold H45,Buckley David67,Campbell Alexander S1,Davis Marcus C8ORCID,Micklem Gos23ORCID,Baker Clare VH1ORCID

Affiliation:

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.

Funder

Biotechnology and Biological Sciences Research Council

Leverhulme Trust

Fisheries Society of the British Isles

National Science Foundation

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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