Odorant-binding proteins in canine anal sac glands indicate an evolutionarily conserved role in mammalian chemical communication

Abstract Background Chemical communication is an important aspect of the behavioural ecology of a wide range of mammals. In dogs and other carnivores, anal sac glands are thought to convey information to conspecifics by secreting a pallet of small volatile molecules produced by symbiotic bacteria. Because these glands are unique to carnivores, it is unclear how their secretions relate to those of other placental mammals that make use of different tissues and secretions for chemical communication. Here we analyse the anal sac glands of domestic dogs to verify the secretion of proteins and infer their evolutionary relationship to those involved in the chemical communication of non-carnivoran mammals. Results Proteomic analysis of anal sac gland secretions of 17 dogs revealed the consistently abundant presence of three related proteins. Homology searches against online databases indicate that these proteins are evolutionary related to ‘odorant binding proteins’ (OBPs) found in a wide range of mammalian secretions and known to contribute to chemical communication. Screening of the dog’s genome sequence show that the newly discovered OBPs are encoded by a single cluster of three genes in the pseudoautosomal region of the X-chromosome. Comparative genomic screening indicates that the same locus is shared by a wide range of placental mammals and that it originated at least before the radiation of extant placental orders. Phylogenetic analyses suggest a dynamic evolution of gene duplication and loss, resulting in large gene clusters in some placental taxa and recurrent loss of this locus in others. The homology of OBPs in canid anal sac glands and those found in other mammalian secretions implies that these proteins maintained a function in chemical communication throughout mammalian evolutionary history by multiple shifts in expression between secretory tissues involved in signal release and nasal mucosa involved in signal reception. Conclusions Our study elucidates a poorly understood part of the biology of a species that lives in close association with humans. In addition, it shows that the protein repertoire underlying chemical communication in mammals is more evolutionarily stable than the variation of involved glands and tissues would suggest.

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Lipocalins in arthropod chemical communication

Genome Biology and Evolution ◽

10.1093/gbe/evab091 ◽

2021 ◽

Author(s):

Jiao Zhu ◽

Alessio Iannucci ◽

Francesca Romana Dani ◽

Wolfgang Knoll ◽

Paolo Pelosi

Keyword(s):

Chemical Communication ◽

Binding Proteins ◽

Aqueous Media ◽

Vomeronasal Organ ◽

Odorant Binding Proteins ◽

Environmental Pressure ◽

Large Numbers ◽

Living Organisms ◽

Odorant Binding ◽

Chemosensory Organs

Abstract Lipocalins represent one of the most successful superfamilies of proteins. Most of them are extracellular carriers for hydrophobic ligands across aqueous media, but other functions have been reported. They are present in most living organisms including bacteria. In animals they have been identified in mammals, molluscs and arthropods; sequences have also been reported for plants. A sub-group of lipocalins, referred to as odorant-binding proteins (OBPs), mediate chemical communication in mammals by ferrying specific pheromones to the vomeronasal organ. So far, these proteins have not been reported as carriers of semiochemicals in other living organisms; instead chemical communication in arthropods is mediated by other protein families structurally unrelated to lipocalins. A search in the databases has revealed extensive duplication and differentiation of lipocalin genes in some species of insects, crustaceans and chelicerates. Their large numbers, ranging from a handful to few dozens in the same species, their wide divergence, both within and between species, and their expression in chemosensory organs suggest that such expansion may have occurred under environmental pressure, thus supporting the hypothesis that lipocalins may be involved in chemical communication in arthropods.

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A Detailed Spatial Expression Analysis of Wing Phenotypes Reveals Novel Patterns of Odorant Binding Proteins in the Soybean Aphid, Aphis glycines

Frontiers in Physiology ◽

10.3389/fphys.2021.702973 ◽

2021 ◽

Vol 12 ◽

Author(s):

Ling Wang ◽

Hang Yin ◽

Zhiguo Zhu ◽

Shuai Yang ◽

Jia Fan

Keyword(s):

Binding Proteins ◽

Expression Patterns ◽

Gene Families ◽

Soybean Aphid ◽

Aphis Glycines ◽

Rapid Expansion ◽

Odorant Binding Proteins ◽

Spatial Expression ◽

Wide Range ◽

Odorant Binding

The wide range of insect niches has led to a rapid expansion of chemosensory gene families as well as their relatively independent evolution and a high variation. Previous studies have revealed some functions for odorant-binding proteins (OBPs) in processes beyond olfaction, such as gustation and reproduction. In this study, a comparative transcriptomic analysis strategy was applied for the soybean aphid, Aphis glycines, focusing on various functional tissues and organs of winged aphids, including the antenna, head, leg, wing, thorax, cauda, and cornicle. Detailed spatial OBP expression patterns in winged and wingless parthenogenetic aphids were detected by RT-qPCR. Twelve OBPs were identified, and three new OBPs in A. glycines are first reported. All OBPs showed comparatively higher expression in sensory organs and tissues, such as the antenna, head, or leg. Additionally, we found some novel expression patterns for aphid OBPs (Beckendorf et al., 2008). Five OBPs exhibited high-expression levels in the cauda and four in the cornicle (Biasio et al., 2015). Three genes (OBP2/3/15) were highly expressed in the wing (Calvello et al., 2003). Two (OBP3/15) were significantly more highly expressed in the wingless thorax than in the winged thorax with the wings removed, and these transcripts were significantly enriched in the removed wings. More details regarding OBP spatial expression were revealed under our strategy. These findings supported the existence of carrier transport functions other than for foreign chemicals and therefore broader ligand ranges of aphid OBPs. It is important for understanding how insect OBPs function in chemical perception as well as their other potential physiological functions.

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