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      A transcriptomic atlas of mammalian olfactory mucosae reveals an evolutionary influence on food odor detection in humans

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          Abstract

          Comparative transcriptomics of olfactory mucosae offers clues into the putative functions of highly abundant ORs in mammals.

          Abstract

          The mammalian olfactory system displays species-specific adaptations to different ecological niches. To investigate the evolutionary dynamics of olfactory sensory neuron (OSN) subtypes across mammalian evolution, we applied RNA sequencing of whole olfactory mucosa samples from mouse, rat, dog, marmoset, macaque, and human. We find that OSN subtypes, representative of all known mouse chemosensory receptor gene families, are present in all analyzed species. Further, we show that OSN subtypes expressing canonical olfactory receptors are distributed across a large dynamic range and that homologous subtypes can be either highly abundant across all species or species/order specific. Highly abundant mouse and human OSN subtypes detect odorants with similar sensory profiles and sense ecologically relevant odorants, such as mouse semiochemicals or human key food odorants. Together, our results allow for a better understanding of the evolution of mammalian olfaction in mammals and provide insights into the possible functions of highly abundant OSN subtypes.

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          Combinatorial receptor codes for odors.

          The discriminatory capacity of the mammalian olfactory system is such that thousands of volatile chemicals are perceived as having distinct odors. Here we used a combination of calcium imaging and single-cell RT-PCR to identify odorant receptors (ORs) for odorants with related structures but varied odors. We found that one OR recognizes multiple odorants and that one odorant is recognized by multiple ORs, but that different odorants are recognized by different combinations of ORs. Thus, the olfactory system uses a combinatorial receptor coding scheme to encode odor identities. Our studies also indicate that slight alterations in an odorant, or a change in its concentration, can change its "code," potentially explaining how such changes can alter perceived odor quality.
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            The olfactory receptor gene superfamily of the mouse

            Olfactory receptor (OR) genes are the largest gene superfamily in vertebrates. We have identified the mouse OR genes from the nearly complete Celera mouse genome by a comprehensive data mining strategy. We found 1,296 mouse OR genes (including 20% pseudogenes), which can be classified into 228 families. OR genes are distributed in 27 clusters on all mouse chromosomes except 12 and Y. One OR gene cluster matches a known locus mediating a specific anosmia, indicating the anosmia may be due directly to the loss of receptors. A large number of apparently functional 'fish-like' Class I OR genes in the mouse genome may have important roles in mammalian olfaction. Human ORs cover a similar 'receptor space' as the mouse ORs, suggesting that the human olfactory system has retained the ability to recognize a broad spectrum of chemicals even though humans have lost nearly two-thirds of the OR genes as compared to mice.
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              Genetic variation in a human odorant receptor alters odour perception.

              Human olfactory perception differs enormously between individuals, with large reported perceptual variations in the intensity and pleasantness of a given odour. For instance, androstenone (5alpha-androst-16-en-3-one), an odorous steroid derived from testosterone, is variously perceived by different individuals as offensive ("sweaty, urinous"), pleasant ("sweet, floral") or odourless. Similar variation in odour perception has been observed for several other odours. The mechanistic basis of variation in odour perception between individuals is unknown. We investigated whether genetic variation in human odorant receptor genes accounts in part for variation in odour perception between individuals. Here we show that a human odorant receptor, OR7D4, is selectively activated in vitro by androstenone and the related odorous steroid androstadienone (androsta-4,16-dien-3-one) and does not respond to a panel of 64 other odours and two solvents. A common variant of this receptor (OR7D4 WM) contains two non-synonymous single nucleotide polymorphisms (SNPs), resulting in two amino acid substitutions (R88W, T133M; hence 'RT') that severely impair function in vitro. Human subjects with RT/WM or WM/WM genotypes as a group were less sensitive to androstenone and androstadienone and found both odours less unpleasant than the RT/RT group. Genotypic variation in OR7D4 accounts for a significant proportion of the valence (pleasantness or unpleasantness) and intensity variance in perception of these steroidal odours. Our results demonstrate the first link between the function of a human odorant receptor in vitro and odour perception.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                July 2019
                31 July 2019
                : 5
                : 7
                : eaax0396
                Affiliations
                [1 ]Sidra Medicine, PO Box 26999, Doha, Qatar.
                [2 ]Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
                [3 ]European Bioinformatics Institute (EMBL-EBI), European Molecular Biology Laboratory, Wellcome Genome Campus, Hinxton,, Cambridge CB10 1SD, UK.
                [4 ]Monell Chemical Senses Center, Philadelphia, PA 19104, USA.
                [5 ]Max Planck Research Unit for Neurogenetics, Max von-Laue-Strasse 4, 60438 Frankfurt, Germany.
                [6 ]Department of ENT-HNS, UZ Leuven, Herestraat 49, 3000 Leuven, Belgium.
                [7 ]Waltham Centre for Pet Nutrition, Leicestershire LE14 4RT, UK.
                [8 ]CRUK Cambridge Institute, University of Cambridge, Cambridge CB2 0RE, UK
                [9 ]Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA.
                Author notes
                [* ]Corresponding author. Email: saraivalmr@ 123456gmail.com (L.R.S.); darren.logan@ 123456effem.com (D.W.L.)
                Author information
                http://orcid.org/0000-0003-4079-0396
                http://orcid.org/0000-0002-6671-1177
                http://orcid.org/0000-0002-9000-4595
                http://orcid.org/0000-0002-5189-2040
                http://orcid.org/0000-0003-4609-6098
                http://orcid.org/0000-0001-5469-9919
                http://orcid.org/0000-0002-9387-3841
                http://orcid.org/0000-0002-5325-7956
                http://orcid.org/0000-0001-9092-0852
                http://orcid.org/0000-0002-5056-4598
                http://orcid.org/0000-0003-1545-5510
                Article
                aax0396
                10.1126/sciadv.aax0396
                6669018
                31392275
                1075817e-9877-4182-9a52-037a30f2849d
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

                This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 February 2019
                : 24 June 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: Grant No. 098051
                Funded by: EMBO Young Investigator Programme;
                Funded by: Sidra Medicine;
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Evolutionary Biology
                Neuroscience
                Evolutionary Biology
                Custom metadata
                Sam Ardiente

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