Molecular basis of ancestral vertebrate electroreception

Bellono, Nicholas W.; Leitch, Duncan B.; Julius, David

doi:10.1038/nature21401

Cited by 91 publications

(132 citation statements)

References 44 publications

(38 reference statements)

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“…Furthermore, given that Cacnb2 seems to be expressed at higher levels in ampullary organs than in neuromasts in paddlefish, it is possible that the voltage-sensing channels include the auxiliary beta subunit Ca v β 2 . (In contrast, deep-sequencing data from skate ampullary organs suggest that Ca v β 1 , encoded by Cacnb1 , might be the auxiliary beta subunit in this species; Bellono et al, 2017.) Testing these hypotheses will require subcellular localization using paddlefish Ca v channel subunit-specific antibodies and/or the optimization of CRISPR/Cas9 in conjunction with larval electroreceptor recordings, in this or related species.…”

Section: Discussionmentioning

confidence: 99%

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

Modrell

Lyne

Carr

et al. 2017

eLife

171

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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.DOI: http://dx.doi.org/10.7554/eLife.24197.001

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Section: Discussionmentioning

confidence: 99%

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

Modrell

Lyne

Carr

et al. 2017

eLife

171

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“…Considering the research of Bellono et al . (, ), it is likely that these hormone‐induced seasonal changes in electroreceptor sensitivity are due, in part, to altered gene expression patterns and molecular modifications to the ion channels within the receptor cells.…”

Section: Physiologymentioning

confidence: 99%

Electroreception in marine fishes: chondrichthyans

Newton

Gill

Kajiura

2019

Journal of Fish Biology

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Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up‐to‐date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.

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“…Atoh1 and other factors are also expressed in and needed for Merkel cell development (Bermingham et al, 2001) and Merkel cells share a mechanotransduction channel [Piezo2 (Woo et al, 2014)] with some hair cells (Wu et al, 2016) indicating the possibility that this highly conserved channel is directly tied into Atoh1 signaling, possibly derived from an ancestral function in epidermal cells (Arendt et al, 2016). Other channels associated with mechanosensory hair cells have recently been identified as being part of the derived non-mechanosensory ‘hair cells’ of the electroreceptive organs, yet another permutation of receptor cell development driven by a nearly identical set of transcription factors (Bellono et al, 2017; Pierce et al, 2008). …”

Section: Introductionmentioning

confidence: 99%

Gene, cell, and organ multiplication drives inner ear evolution

Fritzsch

Elliott

2017

Developmental Biology

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We review the development and evolution of the ear neurosensory cells, the aggregation of neurosensory cells into an otic placode, the evolution of novel neurosensory structures dedicated to hearing and the evolution of novel nuclei and their input dedicated to processing those novel auditory stimuli. The evolution of the apparently novel auditory system lies in duplication and diversification of cell fate transcription regulation that allows variation at the cellular level [transforming a single neurosensory cell into a sensory cell connected to its targets by a sensory neuron as well as diversifying hair cells], organ level [duplication of organ development followed by diversification and novel stimulus acquisition] and brain nuclear level [multiplication of transcription factors to regulate various neuron and neuron aggregate fate to transform the spinal cord into the unique hindbrain organization]. Tying cell fate changes driven by bHLH and other transcription factors into cell and organ changes is at the moment tentative as not all relevant factors are known and their gene regulatory network is only rudimentary understood. Future research can use the blueprint proposed here to provide both the deeper molecular evolutionary understanding as well as a more detailed appreciation of developmental networks. This understanding can reveal how an auditory system evolved through transformation of existing cell fate determining networks and thus how neurosensory evolution occurred through molecular changes affecting cell fate decision processes. Appreciating the evolutionary cascade of developmental program changes could allow identifying essential steps needed to restore cells and organs in the future.

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Molecular basis of ancestral vertebrate electroreception

Cited by 91 publications

References 44 publications

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

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

Electroreception in marine fishes: chondrichthyans

Gene, cell, and organ multiplication drives inner ear evolution

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