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

Syed, Adnan S.; Sharma, Kanika; Policarpo, Maxime; Ferrando, Sara; Casañe, Didier; Korsching, Sigrun I.

doi:10.1093/molbev/msad076

Cited by 5 publications

(3 citation statements)

References 79 publications

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“…Bitter taste receptors had been assumed to originate in bony vertebrates since they had not been found in their sister group (cartilaginous fish, comprising sharks, rays, and chimaeras) nor in the more basal (earlier-derived) jawless fish (lampreys) ( 10 ). However, their immediate sister family are olfactory receptors that do occur also in cartilaginous and jawless fish (vomeronasal receptors type 1/olfactory receptors related to class A, V1Rs/ORAs) ( 12 – 14 ). This phylogenetic relationship suggests an earlier origin for T2Rs.…”

Section: Resultsmentioning

confidence: 99%

A singular shark bitter taste receptor provides insights into the evolution of bitter taste perception

Behrens,

Lang,

Korsching

2023

Proc. Natl. Acad. Sci. U.S.A.

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Many animal and plant species synthesize toxic compounds as deterrent; thus, detection of these compounds is of vital importance to avoid their ingestion. Often, such compounds are recognized by taste 2 receptors that mediate bitter taste in humans. Until now, bitter taste receptors have only been found in bony vertebrates, where they occur as a large family already in coelacanth, a “living fossil” and the earliest-diverging extant lobe-finned fish. Here, we have revisited the evolutionary origin of taste 2 receptors (T2Rs) making use of a multitude of recently available cartilaginous fish genomes. We have identified a singular T2R in 12 cartilaginous fish species (9 sharks, 1 sawfish, and 2 skates), which represents a sister clade to all bony fish T2Rs. We have examined its ligands for two shark species, a catshark and a bamboo shark. The ligand repertoire of bamboo shark represents a subset of that of the catshark, with roughly similar thresholds. Amarogentin, one of the most bitter natural substances for humans, also elicited the highest signal amplitudes with both shark receptors. Other subsets of ligands are shared with basal bony fish T2Rs indicating an astonishing degree of functional conservation over nearly 500 mya of separate evolution. Both shark receptors respond to endogenous steroids as well as xenobiotic compounds, whereas separate receptors exist for xenobiotics both in early- and late-derived bony vertebrates (coelacanth, zebrafish, and human), consistent with the shark T2R reflecting the original ligand repertoire of the ancestral bitter taste receptor at the evolutionary origin of this family.

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Section: Resultsmentioning

confidence: 99%

A singular shark bitter taste receptor provides insights into the evolution of bitter taste perception

Behrens,

Lang,

Korsching

2023

Proc. Natl. Acad. Sci. U.S.A.

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“…In the MOE, the major two neuronal subpopulations are ciliated and microvillous ORNs (Gliem et al, 2013). In the single olfactory sensory epithelium of bony and cartilaginous fishes, trpc2 is expressed in microvillous ORNs (Sato et al, 2005;Syed et al, 2023). In early diverging tetrapods, like amphibians, the expression pattern is in an intermediate state.…”

Section: S100z Expression Pattern Correlates With Microvillous Orns A...mentioning

confidence: 99%

“…Such changes can also result in alterations to the occurrence of cellular properties that are associated with either the main or accessory olfactory system. In cartilaginous fish, the v2r/OlfC family of olfactory receptor genes is dominant over the OR family, and only microvillous ORNs are present in the olfactory organ (Syed et al, 2023).…”

Section: S100z Is Not Associated With the Vno In Xenopusmentioning

confidence: 99%

S100Z is expressed in a lateral subpopulation of olfactory receptor neurons in the main olfactory system of Xenopus laevis

Kahl,

Offner,

Trendel

et al. 2024

Developmental Neurobiology

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In contrast to other S100 protein members, the function of S100 calcium‐binding protein Z (S100Z) remains largely uncharacterized. It is expressed in the olfactory epithelium of fish, and it is closely associated with the vomeronasal organ (VNO) in mammals. In this study, we analyzed the expression pattern of S100Z in the olfactory system of the anuran amphibian Xenopus laevis. Using immunohistochemistry in whole mount and slice preparations of the larval olfactory system, we found exclusive S100Z expression in a subpopulation of olfactory receptor neurons (ORNs) of the main olfactory epithelium (MOE). S100Z expression was not co‐localized with TP63 and cytokeratin type II, ruling out basal cell and supporting cell identity. The distribution of S100Z‐expressing ORNs was laterally biased, and their average number was significantly increased in the lateral half of the olfactory epithelium. The axons of S100Z‐positive neurons projected exclusively into the lateral and intermediate glomerular clusters of the main olfactory bulb (OB). Even after metamorphic restructuring of the olfactory system, S100Z expression was restricted to a neuronal subpopulation of the MOE, which was then located in the newly formed middle cavity. An axonal projection into the ventro‐lateral OB persisted also in postmetamorphic frogs. In summary, S100Z is exclusively associated with the main olfactory system in the amphibian Xenopus and not with the VNO as in mammals, despite the presence of a separate accessory olfactory system in both classes.

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The olfactory system of sharks and rays in numbers

Aicardi,

Bozzo,

Guallart

et al. 2024

The Anatomical Record

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Cartilaginous fishes have large and elaborate olfactory organs, but only a small repertoire of olfactory receptor genes. Here, we quantitatively analyze the olfactory system of 21 species of sharks and rays, assessing many features of the olfactory organ (OOR) (number of primary lamellae, branches of the secondary folds, sensory surface area, and density and number of sensory neurons) and the olfactory bulb (OB) (number of neurons and non‐neuronal cells), and estimate the ratio between the number of neurons in the two structures. We show that the number of lamellae in the OOR does not correlate with the sensory surface area, while the complexity of the lamellar shape does. The total number of olfactory receptor neurons ranges from 30.5 million to 4.3 billion and the total number of OB neurons from 1.5 to 90 million. The number of neurons in the olfactory epithelium is 16 to 158 times higher (median ratio is 46) than the number of neurons in the OB. These ratios considerably exceed those reported in mammals. High convergence from receptor neurons to neurons processing olfactory information, together with the remarkably small olfactory receptor repertoire, strongly suggests that the olfactory system of sharks and rays is well adapted to detect a limited number of odorants with high sensitivity.

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

Cited by 5 publications

References 79 publications

A singular shark bitter taste receptor provides insights into the evolution of bitter taste perception

A singular shark bitter taste receptor provides insights into the evolution of bitter taste perception

S100Z is expressed in a lateral subpopulation of olfactory receptor neurons in the main olfactory system of Xenopus laevis

The olfactory system of sharks and rays in numbers

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