Abstract
The vomeronasal receptor 1 (V1R) are believed to be pheromone receptors in rodents. Here we used computational methods to identify 95 and 62 new putative V1R genes from the draft rat and mouse genome sequence, respectively. The rat V1R repertoire consists of 11 subfamilies, 10 of which are shared with the mouse, while rat appears to lack the H and I subfamilies found in mouse and possesses one unique subfamily (M). The estimations of the relative divergence times suggest that many subfamilies originated after the split of rodents and primates. The analysis also reveals that these clusters underwent an expansion very close to the split of mouse and rat. In addition, maximum likelihood analysis showed that the nonsynonymous and synonymous rate ratio for most of these clusters was much higher than one, suggesting the role of positive selection in the diversification of these duplicated V1R genes. Because V1R are thought to mediate the process of signal transduction in response to pheromone detection, we speculate that the V1R genes have evolved under positive Darwinian selection to maintain the ability to discriminate between large and complex pheromonal mixtures.
Similar content being viewed by others
References
RM Adkins EL Gelke D Rowe RL Honeycutt (2001) ArticleTitleMolecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes Mol Biol Evol 18 777–791 Occurrence Handle1:CAS:528:DC%2BD3MXjtFyktrc%3D Occurrence Handle11319262
RM Adkins AH Walton RL Honeycutt (2003) ArticleTitleHigher-level systematics of rodents and divergence time estimates based on two congruent nuclear genes Mol Phylogenet Evol 26 409–420 Occurrence Handle1:CAS:528:DC%2BD3sXitVKntL8%3D Occurrence Handle12644400
SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389–402 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694
M Anisimova JP Bielawski Z Yang (2001) ArticleTitleAccuracy and power of the likelihood ratio test in detecting adaptive molecular evolution Mol Biol Evol 18 1585–1592 Occurrence Handle1:CAS:528:DC%2BD3MXlslOisLw%3D Occurrence Handle11470850
M Anisimova JP Bielawski Z Yang (2002) ArticleTitleAccuracy and power of bayes prediction of amino acid sites under positive selection Mol Biol Evol 19 950–958 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojur8%3D Occurrence Handle12032251
A Berghard LB Buck (1996) ArticleTitleSensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade J Neurosci 16 909–918 Occurrence Handle1:CAS:528:DyaK28XmsVemsA%3D%3D Occurrence Handle8558259
JP Bielawski KA Dunn G Sabehi O Béàja (2004) ArticleTitleDarwinian adaptation of proteorhodopsin to different light intensities in the marine environment Proc Natl Acad Sci USA 101 14824–14829 Occurrence Handle1:CAS:528:DC%2BD2cXovVyju7Y%3D Occurrence Handle15466697
K Punta ParticleDel T Leinders-Zufall I Rodriguez D Jukam CJ Wysocki S Ogawa F Zufall P Mombaerts (2002) ArticleTitleDeficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes Nature 419 70–74 Occurrence Handle10.1038/nature00955 Occurrence Handle12214233
K Punta ParticleDel A Rothman I Rodriguez P Mombaerts (2000) ArticleTitleSequence diversity and genomic organization of vomeronasal receptor genes in the mouse Genome Res 10 1958–1967 Occurrence Handle11116090
C Dulac R Axel (1995) ArticleTitleA novel family of genes encoding putative pheromone receptors in mammals Cell 83 195–206 Occurrence Handle1:CAS:528:DyaK2MXovVGrtbs%3D Occurrence Handle7585937
Felsenstein (1985) ArticleTitleConfidence limits on phytogenies: an approach using the bootstrap Evolution 39 783–791
D Giorgi C Friedman BJ Trask S Rouquier (2000) ArticleTitleCharacterization of nonfunctional VIR-like pheromone receptor sequences in human Genome Res 10 1979–1985 Occurrence Handle1:CAS:528:DC%2BD3MXjs1E%3D Occurrence Handle11116092
N Goldman Z Yang (1994) ArticleTitleA codon-based model of nucleotide substitution for protein-coding DNA sequences Mol Biol Evol 11 725–736 Occurrence Handle1:CAS:528:DyaK2cXmt1eit70%3D Occurrence Handle7968486
S Guindon O Gascuel (2003) ArticleTitleA simple, fast, and accurate algorithm to estimate large phytogenies by maximum likelihood Syst Biol 52 IssueID5 696–704 Occurrence Handle10.1080/10635150390235520 Occurrence Handle14530136
M Halpern (1987) ArticleTitleThe organization and function of the vomeronasal system Annu Rev Neurosci 10 325–362 Occurrence Handle1:STN:280:BiiC1czhtlQ%3D Occurrence Handle3032065
M Hasegawa H Kishino T Yano (1985) ArticleTitleDating of the human-ape splitting by a molecular clock of mitochondrial DNA J Mol Evol 22 160–174 Occurrence Handle1:CAS:528:DyaL2MXmtFSns7g%3D Occurrence Handle3934395
DT Haydon AD Bastos NJ Knowles AR Samuel (2001) ArticleTitleEvidence for positive selection in foot-and-mouth disease virus capsid genes from field isolates Genetics 157 7–15 Occurrence Handle1:CAS:528:DC%2BD3MXhtFKht74%3D Occurrence Handle11139487
G Herrada C Dulac (1997) ArticleTitleA novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution Cell 90 763–737 Occurrence Handle1:CAS:528:DyaK2sXlvFKmuro%3D Occurrence Handle9288755
AL Hughes MK Hughes (1993) ArticleTitleAdaptive evolution in the rat olfactory receptor gene family J Mol Evol 36 249–54 Occurrence Handle1:CAS:528:DyaK3sXhs1els70%3D Occurrence Handle8483163
C Jia M Halpern (1996) ArticleTitleSubclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb Brain Res 719 117–128 Occurrence Handle1:CAS:528:DyaK28XjsVOgs7Y%3D Occurrence Handle8782871
TH Jukes CR Cantor (1969) Evolution of protein molecules HN Munro (Eds) Mammalian protein metabolisrm Academic Press New York 21–132
EB Keverne (1999) ArticleTitleThe vomeronasal organ Science 286 716–720 Occurrence Handle1:CAS:528:DyaK1MXntFWitrw%3D Occurrence Handle10531049
M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 167 111–120
S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: molecular evolutionary genetics analysis software Bioinformatics 17(12) 1244–1245
RP Lane T Cutforth R Axel L Hood BJ Trask (2002) ArticleTitleSequence analysis of mouse vomeronasal receptor gene clusters reveals common promoter motifs and a history of recent expansion Proc Natl Acad Sci USA 99 291–296 Occurrence Handle1:CAS:528:DC%2BD38Xlt1Cmtw%3D%3D Occurrence Handle11752409
RP Lane J Young T Newman BJ Trask (2004) ArticleTitleSpecies specificity in rodent pheromone receptor repertoires Genome Res 14 603–608 Occurrence Handle1:CAS:528:DC%2BD2cXjt1yjtr0%3D Occurrence Handle15060001
H Matsunami LB Buck (1997) ArticleTitleA multigene family encoding a diverse array of putative pheromone receptors in mammals Cell 90 775–784 Occurrence Handle1:CAS:528:DyaK2sXlvFKmurs%3D Occurrence Handle9288756
EC Metz R Robles-Sikisaka VD Vacquier (1998) ArticleTitleNonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA Proc Natl Acad Sci USA 95 10676–10681 Occurrence Handle1:CAS:528:DyaK1cXlvFWhurs%3D Occurrence Handle9724763
J Ngai MM Dowling L Buck R Axel A Chess (1993) ArticleTitleThe family of genes encoding odorant receptors in the channel catfish Cell 72 657–666 Occurrence Handle1:CAS:528:DyaK3sXisVyru7w%3D Occurrence Handle7916654
R Nielsen Z Yang (1998) ArticleTitleLikelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene Genetics 148 929–936 Occurrence Handle1:CAS:528:DyaK1cXks1eitr8%3D Occurrence Handle9539414
C O’Huigin WH Li (1992) ArticleTitleThe molecular clock ticks regularly in muroid rodents and hamsters J Mol Evol 35 377–384 Occurrence Handle1:CAS:528:DyaK38XmtlSrtbo%3D Occurrence Handle1487823
E Pantages C Dulac (2000) ArticleTitleA novel family of candidate pheromone receptors in mammals Neuron 28 835–845 Occurrence Handle1:CAS:528:DC%2BD3MXis1Kjtw%3D%3D Occurrence Handle11163270
InstitutionalAuthorNameRat Genome Sequencing Consortium (2004) ArticleTitleGenome sequence of the Brown Norway rat yields insights into mammalian evolution Nature 428 493–521
I Rodriguez K Punta ParticleDel A Rothman T Ishii P Mombaerts (2002) ArticleTitleMultiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors Nat Neurosci 5 134–140 Occurrence Handle1:CAS:528:DC%2BD38XhtFGmurc%3D Occurrence Handle11802169
I Rodriguez CA Greer MY Mok P Mombaerts (2000) ArticleTitleA putative pheromone receptor gene expressed in human olfactory mucosa Nat Genet 26 18–19 Occurrence Handle1:CAS:528:DC%2BD3cXmsVKkuro%3D Occurrence Handle10973240
I Rodriguez P Mombaerts (2002) ArticleTitleNovel human vomeronasal receptor-like genes reveal species-specific families Curr Biol 12 R409–R411 Occurrence Handle1:CAS:528:DC%2BD38XlsVyjtr0%3D Occurrence Handle12123587
WL Roelofs AP Rooney (2003) ArticleTitleMolecular genetics and evolution of pheromone biosynthesis in Lepidoptera Proc Natl Acad Sci USA 100 9179–9184 Occurrence Handle1:CAS:528:DC%2BD3sXmtlyksbs%3D Occurrence Handle12876197
NJ Ryba R Tirindelli (1997) ArticleTitleA new multigene family of putative pheromone receptors Neuron 19 371–379 Occurrence Handle1:CAS:528:DyaK2sXlvFensLo%3D Occurrence Handle9292726
H Saito ML Mimmack EB Keverne J Kishimoto PC Emson (1998) ArticleTitleIsolation of mouse vomeronasal receptor genes and their co-localization with specific G-protein messenger RNAs Brain Res Mol Brain Res 60 215–227 Occurrence Handle1:CAS:528:DyaK1cXmtFWnsbg%3D Occurrence Handle9757043
N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015
S Sawyer (1989) ArticleTitleStatistical tests for detecting gene conversion Mol Biol Evol 6 526–538 Occurrence Handle1:CAS:528:DyaL1MXlvFWhtb4%3D Occurrence Handle2677599
P Shi J Zhang H Yang YP Zhang (2003) ArticleTitleAdaptive diversification of bitter taste receptor genes in Mammalian evolution Mol Biol Evol 20 805–814 Occurrence Handle1:CAS:528:DC%2BD3sXkvFCnsr4%3D Occurrence Handle12679530
MS Springer WJ Murphy E Eizirik SJ O’Brien (2003) ArticleTitlePlacental mammal diversification and the Cretaceous-Tertiary boundary Proc Natl Acad Sci USA 100 1056–1061 Occurrence Handle1:CAS:528:DC%2BD3sXhtF2gtrw%3D Occurrence Handle12552136
WJ Swanson VD Vacquier (2002) ArticleTitleThe rapid evolution of reproductive proteins Nat Rev Genet 3 137–144 Occurrence Handle10.1038/nrg733 Occurrence Handle1:CAS:528:DC%2BD38XhsV2ntLY%3D Occurrence Handle11836507
N Takezaki A Rzhetsky M Nei (1995) ArticleTitlePhylogenetic test of the molecular clock and linearized trees Mol Biol Evol 12 823–833 Occurrence Handle1:CAS:528:DyaK2MXns1yqsbg%3D Occurrence Handle7476128
JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417
CJ Wysocki JJ Lepri (1991) ArticleTitleConsequences of removing the vomeronasal organ J Steroid Biochem Mol Biol 39 661–669 Occurrence Handle1:STN:280:By6A28boslY%3D Occurrence Handle1892795
Z Yang (1997) ArticleTitlePAML: a program package for phylogenetic analysis by maximum likelihood Comput Appl Biosci 13 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129
Z Yang JP Bielawski (2000) ArticleTitleStatistical methods for detecting molecular adaptation Trends Ecol Evol 15 496–503 Occurrence Handle11114436
Z Yang R Nielsen (2002) ArticleTitleCodon-substitution models for detecting molecular adaptation at individual sites along specific lineages Mol Biol Evol 19 908–917 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtbk%3D Occurrence Handle12032247
J Zhang (2004) ArticleTitleFrequent false detection of positive selection by the likelihood method with branch-site models Mol Biol Evol 21 1332–1339 Occurrence Handle1:CAS:528:DC%2BD2cXltlKls7c%3D Occurrence Handle15014150
J Zhang DM Webb (2003) ArticleTitleEvolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates Proc Natl Acad Sci USA 100 8337–8341 Occurrence Handle10.1073/pnas.1331721100 Occurrence Handle1:CAS:528:DC%2BD3sXlsFGnt70%3D Occurrence Handle12826614
Acknowledgments
We thank Katherine A. Dunn and two anonymous reviewers for constructive comments. This work was supported by grants from the Chinese Academy of Sciences (KSCX2-1-05), the National Natural Science Foundation of China (30430110 and 30021004), and the Program for Key International S & T Cooperation Project of P.R. China (2001CB711103) to Y.P.Z, a startup fund from Dalhousie Unievrsity to J.P.B., and a grant from the Genome Atlantic Centre of Genome Canada to J.P.B.
Author information
Authors and Affiliations
Corresponding author
Additional information
Reviewing Editor: Dr. Rasmus Nielsen
Rights and permissions
About this article
Cite this article
Shi, P., Bielawski, J.P., Yang, H. et al. Adaptive Diversification of Vomeronasal Receptor 1 Genes in Rodents. J Mol Evol 60, 566–576 (2005). https://doi.org/10.1007/s00239-004-0172-y
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00239-004-0172-y