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Evolutionary Dynamics of Olfactory Receptor Genes in Drosophila Species Evolutionary dynamics of olfactory receptor genes in Drosophila species Masafumi Nozawa, and Masatoshi Nei PNAS published online Apr 16, 2007; doi:10.1073/pnas.0702133104 This information is current as of April 2007. Supplementary Material Supplementary material can be found at: www.pnas.org/cgi/content/full/0702133104/DC1 This article has been cited by other articles: www.pnas.org#otherarticles E-mail Alerts Receive free email alerts when new articles cite this article - sign up in the box at the top right corner of the article or click here. Rights & Permissions To reproduce this article in part (figures, tables) or in entirety, see: www.pnas.org/misc/rightperm.shtml Reprints To order reprints, see: www.pnas.org/misc/reprints.shtml Notes: Evolutionary dynamics of olfactory receptor genes in Drosophila species Masafumi Nozawa* and Masatoshi Nei* Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University, 328 Mueller Laboratory, University Park, PA 16802 Contributed by Masatoshi Nei, March 7, 2007 (sent for review February 23, 2007) Olfactory receptor (OR) genes are of vital importance for animals Results to find food, identify mates, and avoid dangers. In mammals, the Numbers of OR Genes in Drosophila Species. Our homology search number of OR genes is large and varies extensively among differ- (see Materials and Methods) detected 711 functional, 67 non- ent orders, whereas, in insects, the extent of interspecific variation functional, and 34 partial OR genes in the genomes of 12 appears to be small, although only a few species have been Drosophila species. All species examined have similar numbers of studied. To understand the evolutionary changes of OR genes, we functional OR genes and much smaller numbers of pseudogenes identified all OR genes from 12 Drosophila species, of which the (Table 1). Although simulans, sechellia, persimilis, and virilis evolutionary time is roughly equivalent to that of eutherian show somewhat smaller numbers of functional genes, they have mammals. The results showed that all species examined have larger numbers of pseudogenes and partial genes. Here a partial Ϸ similar numbers ( 60) of functional OR genes. Phylogenetic anal- gene refers to a gene with an open reading frame (ORF) ysis indicated that the ancestral species also had similar numbers truncated at the end of a genomic contig studied. This gene may of genes, but there were frequent gains and losses of genes that therefore become a functional gene when the entire genomic occurred in each evolutionary lineage. It appears that tandem sequence is assembled. Some pseudogenes might also become duplication and random inactivation of duplicate genes are the functional genes later because the nonsense or frameshift mu- major factors of gene number change. However, chromosomal tations identified could be caused by sequencing errors. For rearrangements have contributed to the establishment of genome- these reasons, our estimates of functional genes are likely to be wide distribution of OR genes. These results suggest that the minimums except in melanogaster, where the genome sequence repertoire of OR genes in Drosophila has been quite stable com- is well established. In particular, the Hawaiian fruit fly grim- pared with the mammalian genes. The difference in evolutionary shawi, which has many pseudogenes and partial genes, may turn pattern between Drosophila and mammals can be explained partly out to have the largest number of functional genes. In this by the differences of gene expression mechanisms and partly by connection, it should be mentioned that the gene OR83b (OR49 the environmental and behavioral differences. in our notation) is known to be coexpressed with another OR ͉ ͉ gene in most olfactory receptor neurons (ORNs) (10, 11) and is birth-and-death evolution insect evolution multigene family highly conserved even among different orders of insects (12). Yet, this gene in simulans was judged as a pseudogene because lfactory receptor (OR) genes form one of the largest it contained a stop codon. However, if we consider the functional Omultigene families in animals, and the number of genes importance of this gene, the stop codon is likely to have occurred varies extensively among different mammalian orders (Ϸ400– because of sequencing errors. We have therefore decided to 1,200 genes) (1, 2). Insects also have many OR genes, but these regard it as a functional gene in this paper. Furthermore, the genes are remotely related to vertebrate OR genes, and there is previous study showed that melanogaster has 62 functional OR virtually no sequence similarity between them (3). In addition to genes (4), but we regarded one of them (OR85e or OR55)asa the extensive sequence divergence, there is a structural differ- pseudogene because of large deletions. ence between insect and vertebrate OR genes. Both of the genes belong to the G protein-coupled receptor gene superfamily, but Chromosomal Locations of OR Genes and Their Phylogenetic Relation- insect OR genes contain introns (4) whereas vertebrate OR ships. Fig. 1 shows the chromosomal locations of OR genes in genes have no introns in the protein-coding region (5). OR genes melanogaster, yakuba, and pseudoobscura, whose genome se- have been studied in a few insect species, and it has been quences are better assembled than others. OR genes are num- reported that fruit flies (4), mosquitoes (6), and honey bees (7) bered from the left-hand side of the genome to the right-hand Ϸ Ϸ Ϸ have 60, 80, and 160 genes, respectively. This suggests that side in each species. In all these species, OR genes are widely variation in the number of OR genes is smaller in insects than in distributed in the genome except for the dot chromosome mammals. However, to understand the evolutionary dynamics of (chromosome 4 in melanogaster and yakuba, and chromosome 5 OR genes in insects, we need more information about the gene in pseudoobscura), where no OR gene was observed. Phyloge- repertoire of closely related species. netic analysis of these OR genes revealed their orthologous and Fortunately, draft genome sequences of 12 Drosophila species paralogous relationships among the three species (see Fig. 2 for have been released from the Assembly/Alignment/Annotation a segment of the phylogenetic tree). The orthologous genes (AAA) database. The 12 species are D. melanogaster, D. simu- between melanogaster and yakuba are arranged in the genome in lans, D. sechellia, D. yakuba, D. erecta, D. ananassae, D. pseudoob- scura, D. persimilis, D. willistoni, D. virilis, D. mojavensis, and D. grimshawi (the genus name will be omitted in the following). Author contributions: M. Nozawa and M. Nei designed research; M. Nozawa analyzed data; Molecular data have suggested that these species evolved and and M. Nozawa and M. Nei wrote the paper. diverged during the last 63 million years (MY) (8), which is The authors declare no conflict of interest. somewhat lower than but similar to the divergence times of Abbreviations: GO, gene order; MR, modified reconciled-tree; OR, olfactory receptor; ORN, eutherian mammals (Ͻ100 MY) (9). This allows us to compare olfactory receptor neuron. the evolutionary dynamics of OR genes of Drosophila and *To whom correspondence may be addressed. E-mail: [email protected] or [email protected]. mammals. We have therefore conducted an evolutionary study This article contains supporting information online at www.pnas.org/cgi/content/full/ of OR genes from these 12 Drosophila species. The results 0702133104/DC1. obtained are presented in this article. © 2007 by The National Academy of Sciences of the USA 7122–7127 ͉ PNAS ͉ April 24, 2007 ͉ vol. 104 ͉ no. 17 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0702133104 Table 1. Numbers of OR genes in the 12 Drosophila species melanogaster, pseudoobscura (subgenus Sophophora), and virilis Subgenus Species Funct Pseudo Partial Total (subgenus Drosophila). The melanogaster gene OR83b (OR49) and its orthologs from different species were used as outgroups, Sophophora D. melanogaster 61 1 0 62 because the gene is known to have diverged from other OR genes D. simulans 52 4 10 66 a long time ago (4) and have a function different from other OR D. sechellia 54 6 2 62 genes (10, 11). OR genes of each species do not form a D. yakuba 63 0 1 64 species-specific clade but are scattered throughout the tree. We D. erecta 61 1 1 63 classified OR genes into 15 phylogenetic clades (A–O), each of D. ananassae 66 4 3 73 which was defined as the largest cluster of similar genes sup- D. pseudoobscura 64 8 0 72 ported by a bootstrap value of Ն80%. These clades remained D. persimilis 52 12 3 67 unchanged even in the tree constructed for all functional OR D. willistoni 65 7 3 75 genes from the 12 Drosophila species [supporting information (SI) Drosophila D. virilis 53 8 1 62 Fig. 7]. Because all these clades contained OR genes from the D. mojavensis 59 4 0 63 Sophophora and Drosophila species, they must have existed in the D. grimshawi 61 12 10 83 most recent common ancestor (MRCA) of these subgenera. The numbers of genes for the 15 phylogenetic clades in each Funct, functional genes; Pseudo, pseudogenes; Partial, partial genes. of the 12 Drosophila species are presented in Table 2. The number of OR genes varies considerably among these clades, essentially the same order. The genomic arrangement of OR clade L having the largest number of genes. In all species, clade genes in pseudoobscura was quite different from that in the other O has only one gene, which is orthologous to OR83b (OR49)in two species apparently because of the gene rearrangements that melanogaster. The genes belonging to this clade are distantly occurred in the past. However, Fig. 2 indicates that pseudoob- related to other OR genes (Fig. 4). There are some other clades, scura almost always has a gene orthologous to the OR genes from which contain only one or two genes, but it is uncertain whether the other two species.
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