scholarly journals A unified nomenclature for vertebrate olfactory receptors

2019 ◽  
Author(s):  
Tsviya Olender ◽  
Tamsin E.M. Jones ◽  
Michal Twik ◽  
Elspeth Bruford ◽  
Doron Lancet

Abstract Background Olfactory receptors (ORs) are G protein-coupled receptors with a crucial role in odor detection. A typical mammalian genome harbors ~1000 OR genes and pseudogenes; however, different gene duplication/deletion events have occurred in each species, resulting in complex orthology relationships. While the human OR nomenclature is widely accepted and based on phylogenetic classification into 18 families and further into subfamilies, for other mammals different and multiple nomenclature systems are currently in use, thus concealing important evolutionary and functional insights. Results Here we describe the Mutual Maximum Similarity (MMS) algorithm, a systematic classifier for assigning a human-centric nomenclature to any OR gene based on inter-species hierarchical pairwise similarities. MMS was applied to the OR repertoires of seven mammals and zebrafish. Altogether, we assigned symbols to 10,249 ORs. This nomenclature is supported by both phylogenetic and synteny analyses. The availability of a unified nomenclature provides a framework for diverse studies, where textual symbol comparison allows immediate identification of potential ortholog groups as well as species-specific expansions/deletions; for example, Or52e5 and Or52e5b represent a rat-specific duplication of OR52E5 . Another example is the complete absence of OR subfamily OR6Z among primate OR symbols. In other mammals, OR6Z members are located in one genomic cluster, suggesting a large deletion in the great ape lineage. An additional 14 mammalian OR subfamilies are missing from the primate genomes. While in chimpanzee 87% of the symbols were identical to human symbols, this number decreased to ~50% in dog and cow and to ~30% in rodents, reflecting the adaptive changes of the OR gene superfamily across diverse ecological niches. Application of the proposed nomenclature to zebrafish revealed similarity to mammalian ORs that could not be detected from the current zebrafish olfactory receptor gene nomenclature. Conclusions We have consolidated a unified standard nomenclature system for the vertebrate OR superfamily. The new nomenclature system will be applied to cow, horse, dog and chimpanzee by the Vertebrate Gene Nomenclature Committee and its implementation is currently under consideration by other relevant species-specific nomenclature committees.

2020 ◽  
Author(s):  
Tsviya Olender ◽  
Tamsin E.M. Jones ◽  
Elspeth Bruford ◽  
Doron Lancet

Abstract Background Olfactory receptors (ORs) are G protein-coupled receptors with a crucial role in odor detection. A typical mammalian genome harbors ~1000 OR genes and pseudogenes; however, different gene duplication/deletion events have occurred in each species, resulting in complex orthology relationships. While the human OR nomenclature is widely accepted and based on phylogenetic classification into 18 families and further into subfamilies, for other mammals different and multiple nomenclature systems are currently in use, thus concealing important evolutionary and functional insights. Results Here we describe the Mutual Maximum Similarity (MMS) algorithm, a systematic classifier for assigning a human-centric nomenclature to any OR gene based on inter-species hierarchical pairwise similarities. MMS was applied to the OR repertoires of seven mammals and zebrafish. Altogether, we assigned symbols to 10,249 ORs. This nomenclature is supported by both phylogenetic and synteny analyses. The availability of a unified nomenclature provides a framework for diverse studies, where textual symbol comparison allows immediate identification of potential ortholog groups as well as species-specific expansions/deletions; for example, Or52e5 and Or52e5b represent a rat-specific duplication of OR52E5 . Another example is the complete absence of OR subfamily OR6Z among primate OR symbols. In other mammals, OR6Z members are located in one genomic cluster, suggesting a large deletion in the great ape lineage. An additional 14 mammalian OR subfamilies are missing from the primate genomes. While in chimpanzee 87% of the symbols were identical to human symbols, this number decreased to ~50% in dog and cow and to ~30% in rodents, reflecting the adaptive changes of the OR gene superfamily across diverse ecological niches. Application of the proposed nomenclature to zebrafish revealed similarity to mammalian ORs that could not be detected from the current zebrafish olfactory receptor gene nomenclature. Conclusions We have consolidated a unified standard nomenclature system for the vertebrate OR superfamily. The new nomenclature system will be applied to cow, horse, dog and chimpanzee by the Vertebrate Gene Nomenclature Committee and its implementation is currently under consideration by other relevant species-specific nomenclature committees.


2019 ◽  
Author(s):  
Luis R. Saraiva ◽  
Fernando Riveros-McKay ◽  
Massimo Mezzavilla ◽  
Eman H. Abou-Moussa ◽  
Charles J. Arayata ◽  
...  

ABSTRACTThe mammalian olfactory system displays species-specific adaptations to different ecological niches. To investigate the evolutionary dynamics of olfactory sensory neuron (OSN) sub-types across 95 million years of 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 (ORs) are distributed across a large dynamic range and that homologous subtypes can be either highly abundant across all species or species/order-specific. Interestingly, 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. Taken 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 in mouse and human.


2019 ◽  
Vol 5 (7) ◽  
pp. eaax0396 ◽  
Author(s):  
Luis R. Saraiva ◽  
Fernando Riveros-McKay ◽  
Massimo Mezzavilla ◽  
Eman H. Abou-Moussa ◽  
Charles J. Arayata ◽  
...  

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.


2020 ◽  
Author(s):  
Snehal D. Karpe ◽  
Vikas Tiwari ◽  
Sowdhamini Ramanathan

AbstractInsect Olfactory Receptors (ORs) are diverse family of membrane protein receptors responsible for most of the insect olfactory perception and communication, and hence they are of utmost importance for developing repellents or pesticides. Hence, accurate gene prediction of insect ORs from newly sequenced genomes is an important but challenging task. We have developed a dedicated web-server, ‘insectOR’, to predict and validate insect OR genes using multiple gene prediction algorithms, accompanied by relevant validations. It is possible to employ this sever nearly automatically and perform rapid prediction of the OR gene loci from thousands of OR-protein-to-genome alignments, resolve gene boundaries for tandem OR genes and refine them further to provide more complete OR gene models. InsectOR outperformed the popular genome annotation pipelines (MAKER and NCBI eukaryotic genome annotation) in terms of overall sensitivity at base, exon and locus level, when tested on two distantly related insect genomes. It displayed more than 95% nucleotide level precision in both tests. Finally, given the same input data and parameters, InsectOR missed less than 2% gene loci, in contrast to 55% loci missed by MAKER for Drosophila melanogaster. The web-server is freely available on the web at http://caps.ncbs.res.in/insectOR/. All major browsers are supported. Website is implemented in Python with Jinja2 for templating and bootstrap framework which uses HTML, CSS and JavaScript/Ajax. The core pipeline is written in Perl.


2019 ◽  
Vol 44 (9) ◽  
pp. 705-720
Author(s):  
James E Farber ◽  
Robert P Lane

Abstract Olfactory neuronal function depends on the expression and proper regulation of odorant receptor (OR) genes. Previous studies have identified 54 putative intergenic enhancers within or flanking 40 mouse OR clusters. At least 2 of these putative enhancers have been shown to regulate the expression of a small subset of proximal OR genes. In recognition of the large size of the mouse OR gene family (~1400 OR genes distributed across multiple chromosomal loci), it is likely that there remain many additional not-as-yet discovered OR enhancers. We utilized 23 of the previously identified enhancers as a training set (TS) and designed an algorithm that combines a broad range of epigenetic criteria (histone-3-lysine-4 monomethylation, histone-3-lysine-79 trimethylation, histone-3-lysine-27 acetylation, and DNase hypersensitivity) and genetic criteria (cross-species sequence conservation and transcription-factor binding site enrichment) to more broadly search OR gene clusters for additional candidates. We identified 181 new candidate enhancers located at 58 (of 68) mouse OR loci, including 25 new candidates identified by stringent search criteria whose signal strengths are not significantly different from the 23 previously characterized OR enhancers used as the TS. Additionally, we compared OR enhancer versus generic enhancer features in order to evaluate likelihoods that new enhancer candidates specifically function in OR regulation. We found that features distinguishing OR-specific function are significantly more evident for enhancer candidates located within OR clusters as compared with those in flanking regions.


2019 ◽  
Author(s):  
If Barnes ◽  
Ximena Ibarra-Soria ◽  
Stephen Fitzgerald ◽  
Jose Gonzalez ◽  
Claire Davidson ◽  
...  

Abstract Olfactory receptor (OR) genes are the largest multi-gene family in the mammalian genome, with over 850 in human and nearly 1500 genes in mouse. The expansion of the OR gene repertoire has occurred through numerous duplication events followed by diversification, resulting in a large number of highly similar paralogous genes. These characteristics have made the annotation of the complete OR gene repertoire a complex task. Most OR genes have been predicted in silico and are typically annotated as intronless coding sequences. Here we have developed an expert curation pipeline to analyse and annotate every OR gene in the human and mouse reference genomes. By combining evidence from structural features, evolutionary conservation and experimental data, we have unified the annotation of these gene families, and have systematically determined the protein-coding potential of each locus. We have defined the non-coding regions of many OR genes, enabling us to generate full-length transcript models. We found that 13 human and 41 mouse OR loci have coding sequences that are split across two exons. These split OR genes are conserved across mammals, and are expressed at the same level as protein-coding OR genes with an intronless coding region. Our findings challenge the long-standing and widespread notion that the coding region of a vertebrate OR gene is contained within a single exon.


2019 ◽  
Author(s):  
If H. A. Barnes ◽  
Ximena Ibarra-Soria ◽  
Stephen Fitzgerald ◽  
Jose M. Gonzalez ◽  
Claire Davidson ◽  
...  

ABSTRACTOlfactory receptor (OR) genes are the largest multi-gene family in the mammalian genome, with over 850 in human and nearly 1500 genes in mouse. The expansion of the OR gene repertoire has occurred through numerous duplication events followed by diversification, resulting in a large number of highly similar paralogous genes. These characteristics have made the annotation of the complete OR gene repertoire a complex task. Most OR genes have been predicted in silico and are typically annotated as intronless coding sequences. Here we have developed an expert curation pipeline to analyse and annotate every OR gene in the human and mouse reference genomes. By combining evidence from structural features, evolutionary conservation and experimental data, we have unified the annotation of these gene families, and have systematically determined the protein-coding potential of each locus. We have defined the non-coding regions of many OR genes, enabling us to generate full-length transcript models. We found that 13 human and 41 mouse OR loci have coding sequences that are split across two exons. These split OR genes are conserved across mammals, and are expressed at the same level as protein-coding OR genes with an intronless coding region. Our findings challenge the long-standing and widespread notion that the coding region of a vertebrate OR gene is contained within a single exon.


2019 ◽  
Vol 286 (1904) ◽  
pp. 20190909 ◽  
Author(s):  
Graham M. Hughes ◽  
John A. Finarelli

The olfactory bulb (OB) ratio is the size of the OB relative to the cerebral hemisphere, and is used to estimate the proportion of the forebrain devoted to smell. In birds, OB ratio correlates with the number of olfactory receptor (OR) genes and therefore has been used as a proxy for olfactory acuity. By coupling OB ratios with known OR gene repertoires in birds, we infer minimum repertoire sizes for extinct taxa, including non-avian dinosaurs, using phylogenetic modelling, ancestral state reconstruction and comparative genomics. We highlight a shift in the scaling of OB ratio to body size along the lineage leading to modern birds, demonstrating variable OR repertoires present in different dinosaur and crown-bird lineages, with varying factors potentially influencing sensory evolution in theropods. We investigate the ancestral sensory space available to extinct taxa, highlighting potential adaptations to ecological niches. Through combining morphological and genomic data, we show that, while genetic information for extinct taxa is forever lost, it is potentially feasible to investigate evolutionary trajectories in extinct genomes.


Author(s):  
Monika Stengl

Reception of chemicals via olfaction and gustation are prerequisites to find, distinguish, and recognize food and mates and to avoid dangers. Several receptor gene superfamilies are employed in arthropod chemosensation: inverse 7-transmembrane (7-TM) gustatory and olfactory receptors (GRs, ORs), 3-TM ionotropic glutamate-related receptors (IRs), receptor-guanylyl cyclases, transient receptor potential ion channels, and epithelial sodium channels. Some of these receptor gene families have ancient origins and expanded in several taxa, producing very large, variant gene families adapted to the respectively relevant odor ligands in species-specific environments. Biochemical and electrophysiological studies in situ as well as molecular genetics found evidence for G-protein-dependent signal transduction cascades for ORs, GRs, and IRs, suggesting that signal amplification is paramount for chemical senses. In contrast, heterologous expression studies argued for primarily ionotropic transduction as a prerequisite to interstimulus intervals in the range of microseconds.


2020 ◽  
Author(s):  
If Barnes ◽  
Ximena Ibarra-Soria ◽  
Stephen Fitzgerald ◽  
Jose Gonzalez ◽  
Claire Davidson ◽  
...  

Abstract Background: Olfactory receptor (OR) genes are the largest multi-gene family in the mammalian genome, with 874 in human and 1483 loci in mouse (including pseudogenes). The expansion of the OR gene repertoire has occurred through numerous duplication events followed by diversification, resulting in a large number of highly similar paralogous genes. These characteristics have made the annotation of the complete OR gene repertoire a complex task. Most OR genes have been predicted in silico and are typically annotated as intronless coding sequences. Results: Here we have developed an expert curation pipeline to analyse and annotate every OR gene in the human and mouse reference genomes. By combining evidence from structural features, evolutionary conservation and experimental data, we have unified the annotation of these gene families, and have systematically determined the protein-coding potential of each locus. We have defined the non-coding regions of many OR genes, enabling us to generate full-length transcript models. We found that 13 human and 41 mouse OR loci have coding sequences that are split across two exons. These split OR genes are conserved across mammals, and are expressed at the same level as protein-coding OR genes with an intronless coding region. Our findings challenge the long-standing and widespread notion that the coding region of a vertebrate OR gene is contained within a single exon.Conclusions: This work provides the most comprehensive curation effort of the human and mouse OR gene repertoires to date. The complete annotation has been integrated into the GENCODE reference gene set, for immediate availability to the research community.


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