Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome
- University of Cambridge, United Kingdom
- The University of Texas at Austin, United States
- Museo Nacional de Ciencias Naturales-MNCN-CSIC, Spain
- Kennesaw State University, 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.
Data availability
-
Data from: Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptomePublicly available at the NCBI Gene Expression Omnibus (accession no: GSE92470).
Article and author information
Author details
Funding
Biotechnology and Biological Sciences Research Council (BB/F00818X/1)
- Clare VH Baker
Leverhulme Trust (RPG-383)
- Clare VH Baker
Fisheries Society of the British Isles (Research Grant)
- Melinda S Modrell
National Science Foundation (IOS 1557857)
- Harold H Zakon
National Science Foundation (IOS 1144965)
- Marcus C Davis
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experiments were performed in accordance with the approved institutional guidelines and regulations of the Institutional Animal Care and Use Committee of Kennesaw State University (approved protocol #12-001).
Reviewing Editor
- Christine Petit, Institut Pasteur, France
Publication history
- Received: December 14, 2016
- Accepted: March 23, 2017
- Accepted Manuscript published: March 27, 2017 (version 1)
- Accepted Manuscript updated: March 31, 2017 (version 2)
- Accepted Manuscript updated: April 3, 2017 (version 3)
- Version of Record published: May 12, 2017 (version 4)
Copyright
© 2017, Modrell et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,154
- Page views
-
- 530
- Downloads
-
- 26
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome
eLife 6:e24197.
https://doi.org/10.7554/eLife.24197
Further reading
-
- Developmental Biology
Macrophages and their precursor cells, monocytes, are the first line of defense of the body against foreign pathogens and tissue damage. Although the origins of macrophages are diverse, some common transcription factors (such as PU.1) are required to ensure proper development of monocytes/macrophages. Here we report that the deficiency of zbtb14, a transcription repressor gene belonging to ZBTB family, leads to an aberrant expansion of monocyte/macrophage population in zebrafish. Mechanistically, Zbtb14 functions as a negative regulator of pu.1, and SUMOylation on a conserved lysine is essential for the repression activity of Zbtb14. Moreover, a serine to phenylalanine mutation found in an acute myeloid leukemia (AML) patient could target ZBTB14 protein to autophagic degradation. Hence, ZBTB14 is a newly identified gene implicated in both normal and malignant myelopoiesis.
-
- Developmental Biology
- Stem Cells and Regenerative Medicine
The neural crest (NC) is an important multipotent embryonic cell population and its impaired specification leads to various developmental defects, often in an anteroposterior (A-P) axial level-specific manner. The mechanisms underlying the correct A-P regionalisation of human NC cells remain elusive. Recent studies have indicated that trunk NC cells, the presumed precursors of childhood tumour neuroblastoma, are derived from neuromesodermal-potent progenitors of the postcranial body. Here we employ human embryonic stem cell differentiation to define how neuromesodermal progenitor (NMP)-derived NC cells acquire a posterior axial identity. We show that TBXT, a pro-mesodermal transcription factor, mediates early posterior NC/spinal cord regionalisation together with WNT signalling effectors. This occurs by TBXT-driven chromatin remodelling via its binding in key enhancers within HOX gene clusters and other posterior regulator-associated loci. This initial posteriorisation event is succeeded by a second phase of trunk HOX gene control that marks the differentiation of NMPs toward their TBXT-negative NC/spinal cord derivatives and relies predominantly on FGF signalling. Our work reveals a previously unknown role of TBXT in influencing posterior NC fate and points to the existence of temporally discrete, cell type-dependent modes of posterior axial identity control.
