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. 2009 Feb;26(2):407-19.
doi: 10.1093/molbev/msn262. Epub 2008 Nov 13.

Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates

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Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates

Wendy E Grus et al. Mol Biol Evol. 2009 Feb.

Abstract

Comparative genomics provides a valuable tool for inferring the evolutionary history of physiological systems, particularly when this information is difficult to ascertain by morphological traits. One such example is the vomeronasal system (VNS), a vertebrate nasal chemosensory system that is responsible for detecting intraspecific pheromonal cues as well as environmental odorants. The morphological components of the VNS are found only in tetrapods, but the genetic components of the system have been found in teleost fish, in addition to tetrapods. To determine when the genetic components of the VNS originated, we searched for the VNS-specific genes in the genomes of two early diverging vertebrate lineages: the sea lamprey from jawless fishes and the elephant shark from cartilaginous fishes. Genes encoding vomeronasal type 1 receptors (V1Rs) and Trpc2, two components of the vomeronasal signaling pathway, are present in the sea lamprey genome, and both are expressed in the olfactory organ, revealing that the genetic components of the present-day VNS existed in the common ancestor of all extant vertebrates. Additionally, all three VNS genes, Trpc2, V1Rs, and vomeronasal type 2 receptors (V2Rs), are found in the elephant shark genome. Because V1Rs and V2Rs are related to two families of taste receptors, we also searched the early diverging vertebrate genomes for taste system genes and found them in the shark genome but not in the lamprey. Coupled with known distributions of the genetic components of the vertebrate main olfactory system, our results suggest staggered origins of vertebrate sensory systems. These findings are important for understanding the evolution of vertebrate sensory systems and illustrate the utility of the genome sequences of early diverging vertebrates for uncovering the evolution of vertebrate-specific traits.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
V1Rs are found in both the sea lamprey and elephant shark genomes and are expressed in the sea lamprey olfactory epithelium. (A) Unrooted NJ tree of 3 sea lamprey, 2 elephant shark, 7 teleost fish (zebrafish and fugu), 21 frog, and 13 mammalian V1Rs. If the T2R taste receptors (black) are assumed to be the outgroup, all V1Rs cluster together. Two zebrafish T2Rs (GenBank BAE78480 and BAE80435) and 13 X. tropicalis T2Rs (GenBank BAE80422-34) are included. The distinction between T2Rs and V1Rs remains if mammalian T2Rs are also included (data not shown). Bootstrap support for each of the four teleost V1R families and for the clade of T2Rs is given. Scale bar shows 0.2 amino acid substitutions per site. The lamprey V1R gene indicated by * is examined for expression in panel B. (B) Sea lamprey V1R expression in the olfactory organ. Presence of cDNAs in all samples is verified by amplification of the actin cDNA. The lack of amplification in 3′RACE of olfactory organ RNA without reverse transcriptase confirmed that the band was not from genomic contamination.
F<sc>IG</sc>. 2.—
FIG. 2.—
V2Rs are present in the elephant shark genome. An unrooted phylogenetic tree of the 7-transmembrane-domain region from 249 frog, 43 zebrafish, 4 tetraodon, 18 fugu, 5 mammalian, and 25 elephant shark V2Rs. The scale bar shows 0.1 amino acid substitutions per site. The unique subfamily of V2R2 is indicated. Bootstrap percentages >70 are shown for clades containing shark V2Rs.
F<sc>IG</sc>. 3.—
FIG. 3.—
Trpc2 is present in the sea lamprey and elephant shark genomes. Phylogenetic reconstruction of (A) sea lamprey Trpc2 exons 13–15 and (B) elephant shark Trpc2 exon 8 with corresponding regions of the Trpc2 from several other vertebrates and other Trpc genes from mouse. The scale bar shows 0.1 amino acid substitutions per site. Bootstrap percentages greater than 70 are shown. (C) Trpc2 is expressed in the sea lamprey olfactory organ. Presence of cDNA in all samples is verified by amplification of sea lamprey actin as shown in figure 1B. The size of the amplified fragment indicates that it is not from genomic contamination of RNA samples. Further evidence came from the observation of no cDNA amplification when reverse transcriptase is absent.
F<sc>IG</sc>. 4.—
FIG. 4.—
Staggered origins of vertebrate chemosensory systems viewed from the origins of their genetic components, based on the currently available genome sequences. Divergence times are based on Blair and Hedges (2005).

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