Repository logo
 

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

Published version
Peer-reviewed

Repository DOI


Change log

Authors

Minařík, Martin 
Modrell, Melinda S 
Gillis, J Andrew 
Campbell, Alexander S 
Fuller, Isobel 

Abstract

jats:pIn electroreceptive jawed vertebrates, embryonic lateral line placodes give rise to electrosensory ampullary organs as well as mechanosensory neuromasts. Previous reports of shared gene expression suggest that conserved mechanisms underlie electroreceptor and mechanosensory hair cell development and that electroreceptors evolved as a transcriptionally related “sister cell type” to hair cells. We previously identified only one transcription factor gene, jats:italicNeurod4</jats:italic>, as ampullary organ-restricted in the developing lateral line system of a chondrostean ray-finned fish, the Mississippi paddlefish (jats:italicPolyodon spathula</jats:italic>). The other 16 transcription factor genes we previously validated in paddlefish were expressed in both ampullary organs and neuromasts. Here, we used our published lateral line organ-enriched gene-set (arising from differential bulk RNA-seq in late-larval paddlefish), together with a candidate gene approach, to identify 25 transcription factor genes expressed in the developing lateral line system of a more experimentally tractable chondrostean, the sterlet (jats:italicAcipenser ruthenus</jats:italic>, a small sturgeon), and/or that of paddlefish. Thirteen are expressed in both ampullary organs and neuromasts, consistent with conservation of molecular mechanisms. Seven are electrosensory-restricted on the head (jats:italicIrx5</jats:italic>, jats:italicIrx3</jats:italic>, jats:italicInsm1</jats:italic>, jats:italicSp5</jats:italic>, jats:italicSatb2</jats:italic>, jats:italicMafa</jats:italic> and jats:italicRorc</jats:italic>), and five are the first-reported mechanosensory-restricted transcription factor genes (jats:italicFoxg1</jats:italic>, jats:italicSox8</jats:italic>, jats:italicIsl1</jats:italic>, jats:italicHmx2</jats:italic> and jats:italicRorb</jats:italic>). However, as previously reported, jats:italicSox8</jats:italic> is expressed in ampullary organs as well as neuromasts in a catshark (jats:italicScyliorhinus canicula</jats:italic>), suggesting the existence of lineage-specific differences between cartilaginous and ray-finned fishes. Overall, our results support the hypothesis that ampullary organs and neuromasts develop via largely conserved transcriptional mechanisms, and identify multiple transcription factors potentially involved in the formation of electrosensory jats:italicversus</jats:italic> mechanosensory lateral line organs.</jats:p>

Description

Peer reviewed: True


Acknowledgements: Thanks to Marek Rodina and Martin Kahanec for their help with sterlet spawns, and Michaela Vazačová for her help with embryo incubation and fixation. Thanks to Tatjana Piotrowski and her lab at the Stowers Institute for Medical Research (Kansas City, MO, United States) and Steve and Pete Kahrs and the Kahrs family (Osage Catfisheries, Inc.) for hosting MSM during paddlefish spawning seasons. Thanks to Christine Hirschberger and Rolf Ericsson for their help with some of the in situ hybridization rounds. Thanks to Nathanael Walker-Hale for advice on phylogenetic analysis.

Keywords

mechanosensory, sterlet, neuromast, paddlefish, lateral line organs, sturgeon, electrosensory, ampullary organ

Journal Title

Frontiers in Cell and Developmental Biology

Conference Name

Journal ISSN

2296-634X

Volume Title

12

Publisher

Frontiers Media SA