Structure and zonal expression of olfactory receptors in the olfactory epithelium of the goat, <i>Capra hircus</i>

Abstract

The mammalian olfactory system employs sophisticated mechanisms to detect and recognize an extensive range of smells. In rodents, the olfactory epithelium (OE), situated within the nasal cavity, mainly comprises four defined endoturbinates and several ectoturbinates. Olfactory receptors (ORs) belong to a large family, comprising over 1,000 genes in rodents, which are expressed in olfactory sensory neurons in the OE that detect odor molecules. The rodent OE is divided into four topographically distinct zones, defined by individual OR distribution. However, although the structural complexity and the zonal organization of mammalian OE may contribute to successfully interpreting olfactory information, it remains poorly understood. In this study, we investigated the nasal cavity structure and zonal organization of the OE in goats. Morphological observations revealed that the goat nasal cavity possessed well-developed endoturbinates and ectoturbinates and had a structure similar to that of rodents and sheep, previously reported in other studies. In situ hybridization was used to analyze the expression pattern of ORs, NADPH:quinone oxidoreductase 1, and olfactory cell adhesion molecules as markers of zonal organization in the goat OE. Based on the expression patterns of these genes, we concluded that the goat OE was divided into four zones. The well-developed structure of the nasal cavity and distribution of each OR in the OE were similar to those found in rodents, suggesting that these features were highly conserved between mammals and may have fundamental roles in discriminating among numerous odor molecules in the environment.

A 3D transcriptomics atlas of the mouse nose sheds light on the anatomical logic of smell

“…Moreover, the results from this study serve as a template to start answering other important questions about olfaction, such as whether Olfr spatial expression maps can encode maps of odor perception. Because the general molecular mechanisms of olfaction, zonal organization of Olfrs , conservation of ligands among Olfr orthologs, and components of olfactory perception are conserved in mammals ( Adipietro et al, 2012 ; Bear et al, 2016 ; Freitag et al, 1995 ; Horowitz et al, 2014 ; Kurian et al, 2021 ; Manoel et al, 2021 ; Octura et al, 2018 ; Saraiva et al, 2019 ; Weth et al, 1996 ), the association we uncovered here between Olfr zones and the solubility of odorants they detect can likely be extrapolated to other mammals, including humans. Finally, the functional logic underlying the mammalian topographic organization of primary receptor neurons and their receptive fields in smell is now starting to be exposed.…”

“…The global transcriptomic landscape of the vertebrate OM is similar between individuals and broadly conserved among different vertebrate species, ranging from zebrafish to human ( Bear et al, 2016 ; Saraiva et al, 2015a , 2019 ). Similarly, the spatial segregation of Olfrs into partially overlapping rings of expression, centered around the midline structure of the OM, is also conserved among vertebrates ( Freitag et al, 1995 ; Horowitz et al, 2014 ; Marchand et al, 2004 ; Miyamichi et al, 2005 ; Octura et al, 2018 ; Ressler et al, 1993 ; Strotmann et al, 1992 ; Vassar et al, 1993 ; Weth et al, 1996 ). While the number of Olfr zones in zebrafish, frog, and salamander still remain unknown ( Freitag et al, 1995 ; Marchand et al, 2004 ; Weth et al, 1996 ), ISH studies suggested that the total number of Olfr expression zones can vary between mammals—ranging from two in macaque ( Horowitz et al, 2014 ) to four in rat ( Vassar et al, 1993 ) and goat ( Octura et al, 2018 ), and between four and nine in mouse ( Miyamichi et al, 2005 ; Ressler et al, 1993 ; Zapiec and Mombaerts, 2020 ).…”

“…Similarly, the spatial segregation of Olfrs into partially overlapping rings of expression, centered around the midline structure of the OM, is also conserved among vertebrates ( Freitag et al, 1995 ; Horowitz et al, 2014 ; Marchand et al, 2004 ; Miyamichi et al, 2005 ; Octura et al, 2018 ; Ressler et al, 1993 ; Strotmann et al, 1992 ; Vassar et al, 1993 ; Weth et al, 1996 ). While the number of Olfr zones in zebrafish, frog, and salamander still remain unknown ( Freitag et al, 1995 ; Marchand et al, 2004 ; Weth et al, 1996 ), ISH studies suggested that the total number of Olfr expression zones can vary between mammals—ranging from two in macaque ( Horowitz et al, 2014 ) to four in rat ( Vassar et al, 1993 ) and goat ( Octura et al, 2018 ), and between four and nine in mouse ( Miyamichi et al, 2005 ; Ressler et al, 1993 ; Zapiec and Mombaerts, 2020 ). While the exact number of Olfr expression zones in OM still remains under debate, our results are consistent with both another recent RNA-seq study ( Tan and Xie, 2018 ) and the largest Olfr ISH study in the mouse OM ( Miyamichi et al, 2005 ), thus supporting the existence of at least five overlapping Olfr expression zones in the mouse nose.…”

A 3D transcriptomics atlas of the mouse olfactory mucosa

“…Because the general molecular mechanisms of olfaction, zonal organization of Olfrs, and components of olfactory perception are conserved in mammals (73)(74)(75)(76)(77), findings from our and other subsequent studies can likely be extrapolated to other mammals, including humans. Finally, the functional logic underlying the topographic organization of primary receptor neurons and their receptive fields in smell is now starting to be exposed.…”

Genetic background of juniper (Juniperus spp.) consumption predicted by fecal near-infrared spectroscopy in divergently selected goats raised in harsh rangeland environments

“…The identification of these genes could provide insights into the molecular mechanisms underlying the high juniper consuming goats’ ability to perceive and tolerate the consumption of juniper. Goats have a complex nasal cavity and presumably a high sensitivity to odors [ 54 ], which may allow them to detect the amount of plant secondary metabolites such as condensed tannins, mono- and sesquiterpenes in juniper and select plants that have lower levels of these defensive chemicals. Goats prefer J. ashei over J. pinchotii [ 44 ] and the former has 30 – 50% less volatile oils than the latter [ 44 , 55 ], and browsed J. ashei has 60% less volatile oils than unbrowsed plants [ 11 ].…”