A Putative Pheromone Receptor Gene Is Expressed in Two Distinct Olfactory Organs in Goats

Wakabayashi, Yoshihiro; Mori, Yuji; Ichikawa, Masumi; Yazaki, Kazumori; Hagino-Yamagishi, Kimiko

doi:10.1093/chemse/27.3.207

Cited by 66 publications

(66 citation statements)

References 20 publications

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“…Second, in comparison to the V1R gene repertoire, the V2R repertoire is frequently lost in terrestrial vertebrates (Fig. 1) (Wakabayashi et al 2002). A recent study identified two types of vomeronasal systems in mammals (Takigami et al 2004).…”

Section: Discussionmentioning

confidence: 99%

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

Shi¹,

Zhang²

2007

Genome Res.

202

235

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Two evolutionarily unrelated superfamilies of G-protein coupled receptors, V1Rs and V2Rs, bind pheromones and "ordinary" odorants to initiate vomeronasal chemical senses in vertebrates, which play important roles in many aspects of an organism's daily life such as mating, territoriality, and foraging. To study the macroevolution of vomeronasal sensitivity, we identified all V1R and V2R genes from the genome sequences of 11 vertebrates. Our analysis suggests the presence of multiple V1R and V2R genes in the common ancestor of teleost fish and tetrapods and reveals an exceptionally large among-species variation in the sizes of these gene repertoires. Interestingly, the ratio of the number of intact V1R genes to that of V2R genes increased by ∼50-fold as land vertebrates evolved from aquatic vertebrates. A similar increase was found for the ratio of the number of class II odorant receptor (OR) genes to that of class I genes, but not in other vertebrate gene families. Because V1Rs and class II ORs have been suggested to bind to small airborne chemicals, whereas V2Rs and class I ORs recognize water-soluble molecules, these increases reflect a rare case of adaptation to terrestrial life at the gene family level. Several gene families known to function in concert with V2Rs in the mouse are absent outside rodents, indicating rapid changes of interactions between vomeronasal receptors and their molecular partners. Taken together, our results demonstrate the exceptional evolutionary fluidity of vomeronasal receptors, making them excellent targets for studying the molecular basis of physiological and behavioral diversity and adaptation.[Supplemental material is available online at www.genome.org.]Olfaction, or nasal chemoreception, plays a critical role in the daily life of vertebrates. The nasal cavity of most air-breathing vertebrates contains two distinct olfactory tissues/organs: the main olfactory epithelium (MOE) and the vomeronasal organ (VNO) (Dulac and Torello 2003). MOE-mediated olfaction and VNO-mediated olfaction use completely different receptors and signal transduction pathways, and excite different regions of the brain (Dulac and Torello 2003). It was initially thought that MOE and VNO have distinct functions, as MOE detects "ordinary" odorants whereas VNO is specialized for detecting pheromones (Dulac 1997;Buck 2000). This view is changing, as several studies suggested that the MOE can also detect pheromones, whereas the VNO can also detect ordinary odorants (Sam et al. 2001;Boehm et al. 2005;Mandiyan et al. 2005;Yoon et al. 2005;Baxi et al. 2006). Here, pheromones refer to a loosely defined class of chemicals that are emitted and sensed by individuals of the same species to elicit sexual/social behaviors and physiological changes. Examples of pheromone-related behaviors and physiological changes include individual recognition, induction of early puberty, block of pregnancy, and male-male aggression (Keverne 1999).The molecular biology of vertebrate olfaction is best understood in the laboratory mouse Mus m...

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Section: Discussionmentioning

confidence: 99%

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

Shi¹,

Zhang²

2007

Genome Res.

202

235

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“…This explanation also seems unlikely, because all V2Rs we identified from dogs and cows were pseudogenes (data not shown). Furthermore, all V2R genes identified from the human and goat genomes are pseudogenes (17). In fact, no functional V2Rs have been reported in nonrodent mammals.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, a goat V1R gene is known to be expressed in the olfactory epithelium (17). Before we can determine the effects of gene loss in V1R superfamily evolution, we must understand the functional difference between family groups.…”

Section: Discussionmentioning

confidence: 99%

“…However, this hypothesis has not been rigorously tested, because the absence of highly conserved regions in V1Rs makes it difficult to design degenerate primers to amplify a large number of genes across a wide taxonomic scale (15,16). Although a few limited studies in selected mammals suggested possible among-species variation in the numbers of V1R genes and pseudogenes (15,17), the extent of this variation and the exact numbers of genes and pseudogenes in these species are unknown. Furthermore, the long-term evolutionary pattern of V1R genes in mammals and other vertebrates remains largely uncharacterized.…”

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Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals

Grus

Shi

Zhang

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

180

209

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Pheromones are chemicals emitted and sensed by conspecifics to elicit social and sexual responses and are perceived in terrestrial vertebrates primarily by the vomeronasal organ (VNO). Pheromone receptors in the mammalian VNO are encoded by the V1R and V2R gene superfamilies. The V1R superfamily contains 187 and 102 putatively functional genes in the mouse and rat, respectively. To investigate whether this large repertoire size is typical among mammals with functional VNOs, we here describe the V1R repertoires of dog, cow, and opossum based on their draft genome sequences. The dog and cow have only 8 and 32 intact V1R genes, respectively. Thus, the intact V1R repertoire size varies by at least 23-fold among placental mammals with functional VNOs. To our knowledge, this size ratio represents the greatest among-species variation in gene family size of all mammalian gene families. Phylogenetic analysis of placental V1R genes suggests multiple losses of ancestral genes in carnivores and artiodactyls and gains of many new genes by gene duplication in rodents, manifesting massive gene births and deaths. We also identify 49 intact opossum V1R genes and discover independent expansions of the repertoire in placentals and marsupials. We further show a concordance between the V1R repertoire size and the complexity of VNO morphology, suggesting that the latter could indicate the sophistication of pheromone communications within species. In sum, our results demonstrate tremendous diversity and rapid evolution of mammalian V1R gene inventories and caution the generalization of VNO biology from rodents to all mammals. evolution ͉ dog ͉ cow ͉ opossum ͉ rodents

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“…More than 50 intact V2R genes were identified from the mouse and rat genomes , whereas no intact V2R genes were found from the human genome (Bjarnadottir et al 2005) and all the V2R genes identified from goats were pseudogenes (Wakabayashi et al 2002). It is therefore possible that the numbers of functional V2R genes in non-rodent placental mammals are quite small.…”

Section: Vomeronasal Receptorsmentioning

confidence: 99%

Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates

2006

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The numbers of functional olfactory receptor (OR) genes in humans and mice are about 400 and 1,000 respectively. In both humans and mice, these genes exist as genomic clusters and are scattered over almost all chromosomes. The difference in the number of genes between the two species is apparently caused by massive inactivation of OR genes in the human lineage and a substantial increase of OR genes in the mouse lineage after the human-mouse divergence. Compared with mammals, fishes have a much smaller number of OR genes. However, the OR gene family in fishes is much more divergent than that in mammals. Fishes have many different groups of genes that are absent in mammals, suggesting that the mammalian OR gene family is characterized by the loss of many group genes that existed in the ancestor of vertebrates and the subsequent expansion of specific groups of genes. Therefore, this gene family apparently changed dynamically depending on the evolutionary lineage and evolved under the birthand-death model of evolution. Study of the evolutionary changes of two gene families for vomeronasal receptors and two gene families for taste receptors, which are structurally similar, but remotely related to OR genes, showed that some of the gene families evolved in the same fashion as the OR gene family. It appears that the number and types of genes in chemosensory receptor gene families have evolved in response to environmental needs, but they are also affected by fortuitous factors.

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A Putative Pheromone Receptor Gene Is Expressed in Two Distinct Olfactory Organs in Goats

Cited by 66 publications

References 20 publications

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals

Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates

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