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

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

doi:10.7554/elife.24197

Cited by 42 publications

(180 citation statements)

References 145 publications

(273 reference statements)

Supporting

Mentioning

171

Contrasting

Order By: Relevance

“…Paddlefish cDNA was generated according to [52], and primers were designed based on transcriptome sequences ( [57]; electronic supplementary material, table S1). PCR products were cloned into pGEM-T Easy (Promega) and sequenced (Genscript).…”

Section: (B) Cloningmentioning

confidence: 99%

Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod

et al. 2017

Self Cite

View full text Add to dashboard Cite

The evolutionary origin of the autopod involved a loss of the fin-fold and associated dermal skeleton with a concomitant elaboration of the distal endoskeleton to form a wrist and digits. Developmental studies, primarily from teleosts and amniotes, suggest a model for appendage evolution in which a delay in the AER-to-fin-fold conversion fuelled endoskeletal expansion by prolonging the function of AER-mediated regulatory networks. Here, we characterize aspects of paired fin development in the paddlefish (a non-teleost actinopterygian) and catshark (chondrichthyan) to explore aspects of this model in a broader phylogenetic context. Our data demonstrate that in basal gnathostomes, the autopod marker co-localizes with the dermoskeleton component to mark the position of the fin-fold, supporting recent work demonstrating a role for in zebrafish fin ray development. Additionally, we show that in paddlefish, the proximal fin and fin-fold mesenchyme share a common mesodermal origin, and that components of the Shh/LIM/Gremlin/Fgf transcriptional network critical to limb bud outgrowth and patterning are expressed in the fin-fold with a profile similar to that of tetrapods. Together these data draw contrast with hypotheses of AER heterochrony and suggest that limb-specific morphologies arose through evolutionary changes in the differentiation outcome of conserved early distal patterning compartments.

show abstract

Section: (B) Cloningmentioning

confidence: 99%

Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod

et al. 2017

Self Cite

View full text Add to dashboard Cite

show abstract

“…Both cell types develop from embryonic lateral line placodes. Paddlefish electrosensory organs express TFs essential for hair cell development and genes required for synaptic transmission specifically at hair cell ribbon synapses, supporting the idea of homology between electroreceptors and hair cells (Modrell et al, 2017). Furthermore, only a few developmental genes have so far been identified as specific either to electrosensory organs or to neuromasts (lateral line organs containing hair cells), highlighting their close relationship.…”

Section: What Is a Cell Type?mentioning

confidence: 79%

Exciting times to study the identity and evolution of cell types

Sachkova

Burkhardt

2019

Development

View full text Add to dashboard Cite

The EMBO/EMBL Symposium on 'The Identity and Evolution of Cell Types' took place in Heidelberg, Germany, on 15-19 May 2019. The symposium, which brought together a diverse group of speakers addressing a wide range of questions in multiple model systems, provided a platform to discuss how the concept of a cell type should be considered in the era of single cell omics techniques and how cell type evolution can be studied.

show abstract

“…It was suggested that the basal membranes contain voltage dependent potassium channels that explain these results, but the gating mechanism was not established with certainty, nor was any specific type of K channel implicated. Similar pheno- Modrell et al [30 ] have recently studied ion channels in the ampullary electroreceptors of the paddlefish which has strong similarities to skate electroreceptors. They found that the pore forming unit is Kv1.5 (Kcna5), which is a fast neuronal potassium channel of the type that would explain the results in skate electroreceptors.…”

Section: Discovery Of Bk In the Ampulla Of Lorenzini Through Moleculamentioning

confidence: 80%

Further studies of ion channels in the electroreceptor of the skate through deep sequencing, cloning and cross species comparisons

Clusin

Shi

et al. 2018

Preprint

View full text Add to dashboard Cite

Our comparative studies seek to understand the structure and function of ion channels in cartilaginous fish that can detect very low voltage gradients in seawater. The principal channels of the electroreceptor include a calcium activated K channel, whose  subunit is Kcnma1, a voltage-dependent calcium channel, Cacna1d, and a relatively uncharacterized K channel which interacts with the calcium channel to produce fast (20 Hz) oscillations. Large conductance calcium-activated K channels (BK) are comprised of four subunits, encoded by Kcnma1 and modulatory  subunits of the Kcnmb class. We recently cloned and published the skate Kcnma1 gene and most of Kcnmb4 derived from using purified mRNA of homogenized isolated electroreceptors. Bellono et al.have recently performed RNA sequencing (RNA-seq) on purified mRNA from skate electroreceptors and found several ion channels including Kcnma1. We searched the the Bellono et al RNA-seq repository for additional channels and subunits. Our most significant findings are the presence of two Shaker type voltage dependent potassium channel sequences which are grouped together as isoforms in the data repository. The larger of these is a skate ortholog of the voltage dependent fast potassium channel Kv1.1, which is expressed at appreciable levels and seems likely to explain the 20 Hz oscillations believed to occur in vivo. The second was more similar to Kv1.5 than to Kv1.1 but was peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/274449 doi: bioRxiv preprint first posted online Mar. 1, 2018; 3 somewhat atypical. We also found a beta subunit sequence (Kcnab2) which appears not to cause fast inactivation due to specific structural features. The new channels and subunits were verified by RT-PCR and the Kv1.1 sequence was confirmed by cloning. We also searched the RNA-seq repository for accessory subunits of the calcium activated potassium channel, Kcnma1, and found a computer generated assembly that contained a complete sequence of its beta subunit, Kcnmb2. Skate Kcnmb2 has a total of 279 amino acids, with 51 novel amino acids at the N-terminus which may play a specific physiological role. This sequence was confirmed by PCR and cloning. However, skate Kcnmb2 is expressed at low levels in the electroreceptor compared to Kcnma1 and skate Kcnmb1 (beta1) is absent. The evolutionary origin of the newly described channels and subunits was studied by aligning skate sequences with human sequences and those found in related fish: the whale shark (R. typus) an elasmobranch, and ghost shark (C.milii). There is also homology with the lamprey, which has electroreceptors. An evolutionary tree is presented. Further research should include focusing on the subcellular locations of these channels in the receptor cells, their gating behavior, and the effects of accessory subunits on gating.. Introduction.

show abstract

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

Cited by 42 publications

References 145 publications

Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod

Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod

Exciting times to study the identity and evolution of cell types

Further studies of ion channels in the electroreceptor of the skate through deep sequencing, cloning and cross species comparisons

Contact Info

Product

Resources

About