Olfactory receptor subgenome and expression in a highly olfactory procellariiform seabird

Abstract Procellariiform seabirds rely on their sense of smell for foraging and homing. Both genomes and transcriptomes yield important clues about how olfactory receptor (OR) subgenomes are shaped by natural and sexual selection, yet no transcriptomes have been made of any olfactory epithelium of any bird species thus far. Here we assembled a high-quality genome and nasal epithelium transcriptome of the Leach’s storm-petrel (Oceanodroma leucorhoa) to extensively characterize their OR repertoire. Using a depth-of-coverage-assisted counting method, we estimated over 160 intact OR genes (∼500 including OR fragments). This method reveals the highest number of intact OR genes and the lowest proportion of pseudogenes compared to other waterbirds studied, and suggests that rates of OR gene duplication vary between major clades of birds, with particularly high rates in passerines. OR expression patterns reveal two OR genes (OR6-6 and OR5-11) highly expressed in adults, and four OR genes (OR14-14, OR14-12, OR10-2, and OR14-9) differentially expressed between age classes of storm-petrels. All four genes differentially expressed between age classes were more highly expressed in chicks compared to adults, suggesting that ORs genes may exhibit ontogenetic specializations. Three highly differentially expressed OR genes also had high copy number ratios, suggesting that expression variation may be linked to copy number in the genome. We provide better estimates of OR gene number by using a copy number-assisted counting method, and document ontogenetic changes in OR gene expression that may be linked to olfactory specialization. These results provide valuable insight into the expression, development, and macroevolution of olfaction in seabirds.

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Olfactory receptor subgenome and expression in a highly olfactory procellariiform seabird

10.1101/723924 ◽

2019 ◽

Author(s):

Simon Yung Wa Sin ◽

Alison Cloutier ◽

Gabrielle Nevitt ◽

Scott V. Edwards

Keyword(s):

Behavioral Ecology ◽

Olfactory Receptor ◽

Genome Mining ◽

Age Groups ◽

Valuable Insight ◽

Oceanodroma Leucorhoa ◽

Olfactory Sense ◽

Or Gene ◽

Leach’S Storm Petrel ◽

Or Genes

AbstractProcellariiform seabirds are known for their well-developed olfactory capabilities, reflected by their large olfactory bulb to brain ratio and olfactory-mediated behaviors. Many species in this clade use olfactory cues for foraging and navigation, and some species can recognize individual-specific odors. Their genomes and transcriptomes may yield important clues about how the olfactory receptor (OR) subgenome was shaped by natural and sexual selection. In this study, we assembled a high-quality Leach’s storm petrel (Oceanodroma leucorhoa) genome to facilitate characterization of the OR repertoire. We also surveyed expressed OR genes through transcriptome analysis of the olfactory epithelium - to our knowledge, the first avian study to interrogate OR diversity in this way. We detected a large number (∼61) of intact OR genes, and identified OR genes under positive selection. In addition, we estimated that this species has the lowest proportion (∼60%) of pseudogenes compared to other waterbirds studied thus far. We show that the traditional annotation-based genome mining method underestimates OR gene number (214) as compared to copy number analysis using depth-of-coverage analysis, which estimated a total of 492 OR genes. By examining OR expression pattern in this species, we identified highly expressed OR genes, and OR genes that were differentially expressed between age groups, providing valuable insight into the development of olfactory capabilities in this and other avian species. Our genomic evidence is consistent with the Leach’s storm petrel’s well-developed olfactory sense, a key sensory foundation for its pelagic lifestyle and behavioral ecology.

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MHC-Linked Olfactory Receptor Loci Exhibit Polymorphism and Contribute to Extended HLA/OR-Haplotypes

Genome Research ◽

10.1101/gr.120400 ◽

2000 ◽

Vol 10 (12) ◽

pp. 1968-1978 ◽

Cited By ~ 1

Author(s):

Anke Ehlers ◽

Stephan Beck ◽

Simon A. Forbes ◽

John Trowsdale ◽

Armin Volz ◽

...

Keyword(s):

Olfactory Receptor ◽

Sequence Data ◽

Allelic Variation ◽

Mate Preferences ◽

Coding Region ◽

Link Type ◽

Or Gene ◽

Hla Haplotypes ◽

A Minor ◽

Or Genes

Clusters of olfactory receptor (OR) genes are found on most human chromosomes. They are one of the largest mammalian multigene families. Here, we report a systematic study of polymorphism of OR genes belonging to the largest fully sequenced OR cluster. The cluster contains 36 OR genes, of which two belong to the vomeronasal 1 (V1-OR) family. The cluster is divided into a major and a minor region at the telomeric end of the HLA complex on chromosome 6. These OR genes could be involved in MHC-related mate preferences. The polymorphism screen was carried out with 13 genes from the HLA-linked OR cluster and three genes from chromosomes 7, 17, and 19 as controls. Ten human cell lines, representing 18 different chromosome 6s, were analyzed. They were from various ethnic origins and exhibited different HLA haplotypes. All OR genes tested, including those not linked to the HLA complex, were polymorphic. These polymorphisms were dispersed along the coding region and resulted in up to seven alleles for a given OR gene. Three polymorphisms resulted either in stop codons (genes hs6M1-4P,hs6M1-17) or in a 16–bp deletion (gene hs6M1-19P), possibly leading to lack of ligand recognition by the respective receptors in the cell line donors. In total, 13 HLA-linked OR haplotypes could be defined. Therefore, allelic variation appears to be a general feature of human OR genes.[The sequence data reported in this paper have been submitted to EMBL under accession nos. AC006137, AC004178, AJ132194, AL022727, AL031983,AL035402, AL035542, Z98744, CAB55431, AL050339, AL035402, AL096770,AL133267, AL121944, Z98745, AL021808, and AL021807.]

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Expert Curation of the Human and Mouse Olfactory Receptor Gene Repertoires Identifies Conserved Coding Regions Split Across Two Exons.

10.21203/rs.2.17248/v1 ◽

2019 ◽

Author(s):

If Barnes ◽

Ximena Ibarra-Soria ◽

Stephen Fitzgerald ◽

Jose Gonzalez ◽

Claire Davidson ◽

...

Keyword(s):

Olfactory Receptor ◽

Receptor Gene ◽

Gene Repertoire ◽

Coding Region ◽

Protein Coding ◽

Coding Sequences ◽

Coding Regions ◽

Or Gene ◽

Or Genes ◽

Human And Mouse

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.

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Expert Curation of the Human and Mouse Olfactory Receptor Gene Repertoires Identifies Conserved Coding Regions Split Across Two Exons

10.1101/774612 ◽

2019 ◽

Author(s):

If H. A. Barnes ◽

Ximena Ibarra-Soria ◽

Stephen Fitzgerald ◽

Jose M. Gonzalez ◽

Claire Davidson ◽

...

Keyword(s):

Olfactory Receptor ◽

Receptor Gene ◽

Gene Repertoire ◽

Coding Region ◽

Protein Coding ◽

Coding Sequences ◽

Coding Regions ◽

Or Gene ◽

Or Genes ◽

Human And Mouse

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.

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Olfactory receptor repertoire size in dinosaurs

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.0909 ◽

2019 ◽

Vol 286 (1904) ◽

pp. 20190909 ◽

Cited By ~ 4

Author(s):

Graham M. Hughes ◽

John A. Finarelli

Keyword(s):

Olfactory Receptor ◽

Ecological Niches ◽

Ancestral State ◽

Repertoire Size ◽

Receptor Repertoire ◽

Olfactory Acuity ◽

Sensory Evolution ◽

Evolutionary Trajectories ◽

Or Gene ◽

Or Genes

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.

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Gene Expression and Functional Analyses of Odorant Receptors in Small Hive Beetles (Aethina tumida)

International Journal of Molecular Sciences ◽

10.3390/ijms21134582 ◽

2020 ◽

Vol 21 (13) ◽

pp. 4582

Author(s):

Yuanzhen Liu ◽

Alexis Beaurepaire ◽

Curtis W. Rogers ◽

Dawn Lopez ◽

Jay D. Evans ◽

...

Keyword(s):

Expression Patterns ◽

Host Finding ◽

Odorant Receptors ◽

Aethina Tumida ◽

Colony Odor ◽

Or Gene ◽

Functional Analyses ◽

Or Genes ◽

Small Hive Beetles ◽

First Time

Olfaction is key to many insects. Odorant receptors (ORs) stand among the key chemosensory receptors mediating the detection of pheromones and kairomones. Small hive beetles (SHBs), Aethina tumida, are parasites of social bee colonies and olfactory cues are especially important for host finding. However, how interactions with their hosts may have shaped the evolution of ORs in the SHB remains poorly understood. Here, for the first time, we analyzed the evolution of SHB ORs through phylogenetic and positive selection analyses. We then tested the expression of selected OR genes in antennae, heads, and abdomens in four groups of adult SHBs: colony odor-experienced/-naive males and females. The results show that SHBs experienced both OR gene losses and duplications, thereby providing a first understanding of the evolution of SHB ORs. Additionally, three candidate ORs potentially involved in host finding and/or chemical communication were identified. Significantly different downregulations of ORs between the abdomens of male and female SHBs exposed to colony odors may reflect that these expression patterns might also reflect other internal events, e.g., oviposition. Altogether, these results provide novel insights into the evolution of SHB ORs and provide a valuable resource for analyzing the function of key genes, e.g., for developing biological control. These results will also help in understanding the chemosensory system in SHBs and other beetles.

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Expert Curation of the Human and Mouse Olfactory Receptor Gene Repertoires Identifies Conserved Coding Regions Split Across Two Exons

10.21203/rs.2.17248/v2 ◽

2020 ◽

Author(s):

If Barnes ◽

Ximena Ibarra-Soria ◽

Stephen Fitzgerald ◽

Jose Gonzalez ◽

Claire Davidson ◽

...

Keyword(s):

Olfactory Receptor ◽

Receptor Gene ◽

Gene Repertoire ◽

Coding Region ◽

Protein Coding ◽

Coding Sequences ◽

Coding Regions ◽

Or Gene ◽

Or Genes ◽

Human And Mouse

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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Spatial patterns of olfactory neurons expressing specific odor receptor genes in 48-hour-old embryos of zebrafish Danio rerio.

Journal of Experimental Biology ◽

10.1242/jeb.200.3.433 ◽

1997 ◽

Vol 200 (3) ◽

pp. 433-443 ◽

Cited By ~ 1

Author(s):

R G Vogt ◽

S M Lindsay ◽

C A Byrd ◽

M Sun

Keyword(s):

Spatial Patterns ◽

Olfactory Epithelium ◽

Expression Patterns ◽

Initial Population ◽

Olfactory Neuron ◽

Olfactory Neurons ◽

Odor Receptor ◽

Or Gene ◽

Or Genes ◽

Specific Odor

Olfactory neurons have a complex phenotype characterized by their expression of a specific odor receptor (OR) gene and their targeting of an equally specific locus in the olfactory bulb. In the adult fish, olfactory neurons expressing specific ORs are broadly distributed in the epithelium, intermingling with neurons expressing other OR phenotypes. This distributed adult pattern has led to the suggestion that olfactory neuron phenotype is determined by a stochastic process, independent of external positional cues. However, when the fish olfactory system is established during embryogenesis it is simple in its organization, with few olfactory neurons and an olfactory epithelium that has not yet folded into the adult morphology. It is possible that positional cues might act in the embryo to establish an initial population and pattern of olfactory neuron phenotypes and that subsequent morphogenesis and neuronal addition lead to the randomized distribution of neurons. To test this possibility, we examined the spatial patterns of olfactory neurons expressing specific OR genes in 48 h embryos, a time of relative simplicity in the developing olfactory epithelium. Three-dimensional plots of neuron distributions were made, and comparison of OR expression patterns were made between right and left epithelia, between individual animals and between different OR genes. The patterns of OR gene expression were not conserved in these comparison. Mathematical analysis of 21 epithelia for the degree of order in the distribution of olfactory neurons argued strongly that the neurons expressing given ORs are randomly distributed in the 48 h embryos. These results are consistent with those observed from adult tissue and support models suggesting that extrinsic positional cues do not have a major role in specifying olfactory neuron phenotypes.

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Expert Curation of the Human and Mouse Olfactory Receptor Gene Repertoires Identifies Conserved Coding Regions Split Across Two Exons

10.21203/rs.2.17248/v3 ◽

2020 ◽

Author(s):

If Habib Ahmed Barnes ◽

Ximena Ibarra-Soria ◽

Stephen Fitzgerald ◽

Jose Manuel Gonzalez ◽

Claire Davidson ◽

...

Keyword(s):

Olfactory Receptor ◽

Receptor Gene ◽

Gene Repertoire ◽

Coding Region ◽

Protein Coding ◽

Coding Sequences ◽

Coding Regions ◽

Or Gene ◽

Or Genes ◽

Human And Mouse

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Expert Curation of the Human and Mouse Olfactory Receptor Gene Repertoires Identifies Conserved Coding Regions Split Across Two Exons.

10.21203/rs.2.17248/v4 ◽

2020 ◽

Author(s):

If Habib Ahmed Barnes ◽

Ximena Ibarra-Soria ◽

Stephen Fitzgerald ◽

Jose Manuel Gonzalez ◽

Claire Davidson ◽

...

Keyword(s):

Olfactory Receptor ◽

Receptor Gene ◽

Gene Repertoire ◽

Coding Region ◽

Protein Coding ◽

Coding Sequences ◽

Coding Regions ◽

Or Gene ◽

Or Genes ◽

Human And Mouse

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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