Spatial organization of olfactory receptor gene choice in the complete V1R-related ORA family of zebrafish

Abstract

The vertebrate sense of smell employs four main receptor families for detection of odors, among them the V1R/ORA family, which is unusually small and highly conserved in teleost fish. Zebrafish possess just seven ORA receptors, enabling a comprehensive analysis of the expression patterns of the entire family. The olfactory organ of zebrafish is representative for teleosts, cup-shaped, with lamella covered with sensory epithelium protruding into the cup from a median raphe. We have performed quantitative in situ hybridization on complete series of horizontal cryostat sections of adult zebrafish olfactory organ, and have analysed the location of ora-expressing cells in three dimensions, radial diameter, laminar height, and height-within-the-organ. We report broadly overlapping, but distinctly different distributions for all ora genes, even for ora3a and ora3b, the most recent gene duplication. Preferred positions in different dimensions are independent of each other. This spatial logic is very similar to previous reports for the much larger families of odorant receptor (or) and V2R-related olfC genes in zebrafish. Preferred positions for ora genes tend to be more central and more apical than those we observed for these other two families, consistent with expression in non-canonical sensory neuron types.

Ancient and Nonuniform Loss of Olfactory Receptor Expression Renders the Shark Nose a De Facto Vomeronasal Organ

“…We also found expression of only one v1r/ora gene in catshark OE, ora2 . This is again different from the situation in zebrafish, where all ora genes show olfactory expression ( Saraiva and Korsching 2007 ; Kowatschew et al 2022 ). The cell type of the ora2 -expressing neurons is unknown, but they could be microvillous neurons, which do express the related family of v1r genes in mammals ( Mombaerts 2004 ).…”

Calcium imaging of adult olfactory epithelium reveals amines as important odor class in fish

“…The laminar height of cell somata within the lamella is significantly different for different cell populations and can thus serve to characterize the responsive cell population. Laminar height was determined as described previously (Kowatschew et al 2022 ) for cells with odor responses and for PCNA-, OMP- and TRPC2-expressing cells (the latter two in transgenic reporter lines OMP:lynRFP and TRPC2:gap-Venus (Sato et al 2005 )). In short, the distance from the basal lamina to cell soma center (h i ) and the total laminar height h 0 at that position were determined, and the ratio h i /h 0 was plotted as empirical cumulative distribution function (ECDF, Feller 1967 ; Wilk and Gnanadesikan 1968 ).…”

“…Amino acid detection is likely mediated by a large group of class C GPCRs, the V2Rs, also named OlfC in teleost fish (DeMaria et al 2013 ). Concerning nucleotide detection, current knowledge points to a single olfactory receptor, adorb (Kowatschew et al 2022 ), which is highly specific for adenosine, generated within the olfactory mucosa through the hydrolysis of ATP (Wakisaka et al ( 2017 ). Recently, in addition to sparse olfactory sensory neuron (OSN) responses to ATP, non-olfactory responses to ATP have been shown in supporting and basal cells of zebrafish (Demirler et al 2020 ), similar to earlier observations made in larval Xenopus (Czesnik et al 2006 ).…”