Zebrafish aversive taste co-receptor is expressed in both chemo- and mechanosensory cells and plays a role in lateral line development

Abstract

Fishes rely on both chemical and tactile senses to orient themselves to avoid predators, and to detect and taste food. This is likely achieved by highly coordinated reception of signals by mechano- and chemosensory receptors in fish. A small co-receptor from zebrafish, receptor activity modifying protein (RAMP)-like triterpene glycoside receptor (RL-TGR), was previously found to be involved in recognition of triterpene glycosides, a family of naturally occurring compounds that act as chemical defenses in various prey species. However, its localization, function, and how it impacts sensory organ development in vivo is not known. Here we show that RL-TGR is expressed in zebrafish in both i) apical microvilli of the chemosensory cells of taste buds including the epithelium of lips and olfactory epithelium, and ii) mechanosensory cells of neuromasts belonging to the lateral line system. Loss-of-function analyses of RL-TGR resulted in significantly decreased number of neuromasts in the posterior lateral line system and decreased body length, suggesting that RL-TGR is involved in deposition and migration of the neuromasts. Collectively, these results provide the first in vivo genetic evidence of sensory cell-specific expression of this unusual co-receptor and reveal its additional role in the lateral line development in zebrafish.

Visualization of the chemical defense molecule formoside binding to sensory structures in a model fish predator

“…2B ). The distribution of the probe was punctate in appearance, accumulating in structures that, based on previous investigation, likely correspond to taste buds ( Mojib et al, 2017 ). Two distinct taste bud morphologies representing the early primordial ( Fig.…”

“…The negative control cyclododecane-BODIPY probe (D) did not localize to chemosensory or mechanosensory structures (D–F). (I) Schematic of the zebrafish neuromast organization (I) ( Mojib et al, 2017 , modified from Ghysen and Dambly-Chaudiere, 2004 ) and (J) confocal microscopy results showing the labeling of different neuromast substructures by formoside-BODIPY and DASPEI. ul, upper lip; ll, lower lip; e, eye; tb, taste bud; oe, olfactory epithelium; nm, neuromast.…”

“…Based on our observation of formoside localization to the zebrafish olfactory epithelium and taste buds ( Figs 2 and 3 ), it is probable that formoside binds specifically to a receptor or multiple receptors on OSNs and taste receptor cells (as well as neuromasts). RL-TGR, a known chemoreceptor for formoside, has been observed to be expressed in these chemosensory and mechanosensory tissues ( Mojib et al, 2017 ). RL-TGR functions in conjunction with a GPCR ( Cohen et al, 2010 ) and the sensory epithelium of the zebrafish olfactory organ contains five described types of olfactory sensory neurons, each of which expresses combinations of GPCR olfactory receptors, responding to odorants through the regulation of cyclic AMP ( Calvo-Ochoa and Byrd-Jacobs, 2019 ).…”

“…The identity of the GPCR with which RL-TGR acts is unknown. However, expression of RL-TGR in zebrafish olfactory epithelium and taste buds supports its involvement in chemical sensing ( Mojib et al, 2017 ).…”

Heat induces multiomic and phenotypic stress propagation in zebrafish embryos

“…3 B) which supports the biological relevance of the measured response. Prior work identified the lateral line as a candidate organ activated by chemical cues ( 31 , 32 ), which led us to compare the expression of genes expressed by SM and in lateral line hair cells. Remarkably, the DEGs in SM are also significantly up-regulated in zebrafish lateral line hair cells in 5-dpf larvae, relative to their expression in neighboring epidermis cells ( z -score = 8.71505; P < 0.0001, Fig.…”