Journal of Heredity Advance Access originally published online on October 3, 2008
Journal of Heredity 2009 100(1):97-105; doi:10.1093/jhered/esn078
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Original Articles |
Reduced X-Linked Rare Polymorphism in Males in Comparison to Females of Drosophila melanogaster
From the Department of Population Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan (Takahashi and Takano-Shimizu); the Department of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka 411-8540, Japan (Tanaka and Takano-Shimizu); the Department of Applied Biology, Graduate School of Science and Technology, Kyoto Institute of Technology, Kyoto 606-8585, Japan (Itoh); the Insect Biomedical Research Center, Kyoto Institute of Technology, Kyoto, 606-8585, Japan (Itoh); the Department of Biosystems Science, Graduate University for Advanced Studies (SOKENDAI), Hayama, Kanagawa 240-0193, Japan (Takano-Shimizu); and the Department of Biological Science, Graduate School of Science, The University of Tokyo, Tokyo 113-8654, Japan (Takano-Shimizu)
Address correspondence to T. Takano-Shimizu at the address above, or e-mail: totakano{at}lab.nig.ac.jp.
Natural selection is assumed to act more strongly on X-linked loci than on autosomal loci because the fitness effect of a recessive mutation on the X chromosome is fully expressed in hemizygous males. Therefore, selection is expected to fix or remove recessive mutations on the X chromosome more efficiently than those on autosomes. However, the assumption that hemizygosity of the X chromosome selectively accelerates changes in allele frequency has not been confirmed directly. To examine this assumption, we investigated current natural selection on X-linked chemoreceptor genes in a natural population of Drosophila melanogaster by comparing nucleotide diversity, linkage disequilibrium (LD), and departure from the neutrality in 4 chemoreceptor genes on 100 X chromosomes each from female and male flies. The general pattern of nucleotide diversity and LD for the genes investigated was similar in females and males. In contrast, males harbored significantly fewer rare polymorphisms defined as singletons and doubletons. When all the gene sequences were concatenated, Tajima's D showed a significant departure from the neutrality in both females and males, whereas Fu and Li's F* value revealed departure only in males. These results suggest that some rare polymorphisms on the X chromosome from females are recessively deleterious and are removed by stronger purifying selection when transferred to hemizygous males.
Key Words: chemoreceptor gene • drosophila melanogaster • natural selection • rare polymorphism • X-linked polymorphism
Sex chromosomes may play a substantial role in sexual selection and reproductive isolation. Based on published data for mammals, drosophilids, and other insects, Reinhold (1998) suggested that the X chromosome has greater influence on sexually selected traits than do the autosomes. The X chromosome is reported to have significant effects on hybrid sterility in drosophilids and other insects (Coyne and Orr 1989; Orr and Coyne 1989; Betancourt et al. 2002). Such disproportionately large effects of the X chromosome may be caused by more rapid accumulation of advantageous mutations on the X chromosome than on the autosomes (Turelli and Orr 1995).
Charlesworth et al. (1987) indeed showed that, if new mutations are recessive or partially recessive, the substitution rate of selectively favorable new mutations is higher for X-linked loci than for autosomal loci. This is because the fitness effect of a recessive mutation on the X chromosome is fully expressed in hemizygous males, and therefore, positive selection is expected to fix advantageous recessive mutations on the X chromosome more efficiently than those on the autosomes. This prediction is the basis of the faster-X hypothesis. For the same reason, purifying selection removes deleterious recessive mutations more efficiently on the X chromosome than on autosomes, leading to a lower substitution rate of the X chromosome than of autosomes. Thus, by comparing the rates of nucleotide substitution on the X chromosome and autosomes, we can evaluate the relative impact of positive selection and of purifying selection on between-species variation in sequences.
Between-species variation is often studied on the basis of the ratio of synonymous and nonsynonymous substitution rates (Ka/Ks). If the majority of nonsynonymous substitutions is driven by positive selection, the Ka/Ks ratio would be higher for X-linked loci than for autosomal loci; the reverse would be the case if purifying selection limits the evolutionary rate of nonsynonymous substitution. For drosophilid flies, several studies showed that the Ka/Ks ratio is higher for X-linked loci than for autosomal loci, supporting the faster-X hypothesis (Thornton and Long 2002, 2004; Counterman et al. 2004); however, Betancourt et al. (2002) and Thornton et al. (2006) found no difference in Ka/Ks ratios between X-linked and autosomal loci. These inconsistent results suggest that either some of the assumptions of the hypothesis are incorrect or that the proportion of mutations fixed by positive selection has been overestimated (Vicoso and Charlesworth 2006).
Both positive selection and purifying selection reduce within-species variation at the linked neutral sites (hitchhiking effect and background selection, respectively); however, the relative effects on the X chromosome and autosomes differ between these 2 types of selection. The hitchhiking model predicts that variation is significantly lower for X-linked loci than for autosomal loci because of stronger positive selection on advantageous recessive mutations on the X chromosome than those on autosomes (MaynardSmith and Haigh 1974). In contrast, the background selection model predicts larger variation of X-linked loci than of autosomal loci due to stronger purifying selection on deleterious recessive mutations on the X chromosome (Aquadro et al. 1994). Begun and Whitley (2000) compared the numbers of nucleotide polymorphisms between the X chromosome and autosomes of Drosophila simulans and detected fewer nucleotide polymorphisms on the X chromosome, suggesting that the hitchhiking effect has a larger effect on neutral variation than does background selection.
X-versus-autosome comparisons are also used to evaluate fitness effects of transposable element insertions in which insertion frequencies at individual sites are generally very low in Drosophila populations (Montgomery et al. 1987). If most transposable element insertions have deleterious recessive effects, transposons should be less abundant on the X chromosome than on the autosomes. In general, X chromosomes tend to harbor fewer transposable elements than do autosomes, although this is not always the case (Montgomery et al. 1987; Charlesworth et al. 1992; Biémont et al. 1994; Bartolomé et al. 2002). Natural selection appears to be the primary force controlling the transposable element copy number, but whether the insertion of a transposable element is itself deleterious is still unclear (Hoogland and Biémont 1996; Charlesworth et al. 1997).
To detect the action of natural selection at the DNA sequence level, intraspecific variation as well as interspecific variation has been studied and compared between genomic regions, loci, chromosomes, or populations (Kreitman and Hudson 1991; Begun and Whitley 2000; Harr et al. 2002), and several statistical methods have been developed to test the neutral expectation (Tajima 1989; Fu and Li 1993; Fay and Wu 2000). Although sequence variation of X chromosomes has never been compared between females and males, it may provide additional insight into the natural selection acting on the X chromosome. Hemizygosity of X chromosomes in males can cause between-sex difference in selection pressure, which, in turn, causes between-sex differences in measures of variation such as nucleotide diversity and linkage disequilibrium (LD). This novel way to detect natural selection on the X chromosome may also be useful to screen target sites of natural selection.
In this article, we studied a natural population of Drosophila melanogaster by comparing nucleotide diversity, LD, and departure from the neutrality between X chromosomes from females and males. If hemizygosity of X has no effect on natural selection and all other conditions are the same between females and males, no sexual difference in the patterns of polymorphism on the X chromosome would be expected. In contrast, under the above-mentioned assumption, the comparison of male and female X chromosomes might reveal a signature profile of accelerated changes in allele frequency in males. This study may shed some light on the action of natural selection, especially its effects on deleterious mutations fluctuating in a finite population with recombination, about which we know very little (Gillespie 2004).
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Flies
Female and male D. melanogaster were collected by banana trap in Kyoto, Japan, in June 2005. Mating scheme to extract X chromosomes from wild-caught flies is shown in Figure 1. For a wild-caught female, an F1 male progeny of each female was used for DNA extraction. For a wild-caught male, each individual was crossed separately to a compound X chromosome strain, C(1)RM, y wa/y w, and F1 male progeny were collected to extract the X chromosome of the parental male. We did this cross in order to amplify its X chromosome and to avoid possible sampling bias. There is a large variation in body size of wild-caught flies. The body size may affect the success rate of polymerase chain reaction (PCR) amplification and then cause sampling bias. By using progeny obtained in the controlled condition, we could avoid this bias as much as possible. In this way, we prepared 100 X chromosomes each from females and males.
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PCR, Sequencing, and Alignment
Genomic DNA was extracted from the male F1 progeny with a GenEluteTM Mammalian Genomic DNA Miniprep Kit (Sigma, St Louis, MO). An approximately 2.5 kb in total containing the chemoreceptor genes Gr5a, Gr8a, Gr10a, and Or10a was amplified by PCR method with the following primer pairs: 5'-CCTCCTGGCAGTTCCTGA-3' and 5'-TCAGCATTATACCGGACACG-3' for Gr5a, 5'-ATTTGGGATTGTGGCAGTTC-3' and 5'-TGCAATCCAGGATGGTCAG-3' for Gr8a, 5'-CCCGGATATTTCTGCTACCAC-3' and 5'-AACAGGGTGTAGAAGTTGGTC-3' for Gr10a, and 5'-TGCTCTATGTGGCCTACACG-3' and 5'-GCCTCAAAGTGCACGGTATT-3' for the region containing both Gr10a and Or10a. The exon–intron structure and sequenced regions are shown in Figure 2. The sequences of the Gr10a and Or10a regions were concatenated and analyzed as a single fragment as follows. PCR amplification reactions were performed with AmpliTaq Gold Polymerase (Applied Biosystems, Foster City, CA) or PrimeSTAR HS DNA Polymerase (TaKaRa BIO Inc., Shiga, Japan). PCR products were purified with a MultiScreen Filter Plate (Millipore, Billerca, CA) and sequenced in both directions with the BigDye Terminator Cycle Sequencing Kit Version 3 and the same primers used for PCR (Applied Biosystems). Sequences were determined with an ABI 3100 Automated Sequencer (Applied Biosystems). The sequences were assembled with Codon Code Aligner version 1.5 (LI-COR, Inc. Lincoln, NE) and aligned with the Clustal W program in MEGA3 (Kumar et al. 2004).
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Analysis
Searches for polymorphic sites and sliding-window analyses of the level of nucleotide diversity (
) were performed with the DnaSP program, version 4.1 (Munte et al. 2005). Because most deleterious and slightly deleterious mutations do not reach high frequency, they should be observed as rare polymorphisms, if at all. Accordingly, we defined rare polymorphisms as singletons and doubletons and compared the numbers of rare polymorphisms specific to females and males. To test the difference in the number of sex-specific rare polymorphisms, we conducted a randomization test. In this test, we first calculated the difference in the number of sex-specific rare polymorphisms as an observed statistic. Sequences of females and males were grouped together and divided randomly into 2 groups of equal size. The numbers of group-specific rare polymorphisms were then counted, and the difference between the groups was calculated. This process of randomization was repeated 1000 times, and the P value was calculated by comparing the observed statistics to the distribution of the statistics generated by randomization. In the randomization test, we treated each sequence data as a unit of randomization, which allows us to evaluate the statistical significance correctly even when rare polymorphisms are distributed nonrandomly among chromosomes. The index of LD, r2, was calculated with the DnaSP program (Munte et al. 2005). Because of difficulties in interpretation, we excluded rare polymorphisms and trinucleotide segregating sites from this analysis. To test the difference between the degree of LD on X chromosomes from females and males, we repeated the randomization test. In this case, the difference in the average r2 between females and males was used as the test statistic. The process of randomization was repeated 1000 times.
Neutrality indices Tajima's D and Fu and Li's F* (Tajima 1989; Fu and Li 1993) were calculated for each region and for the concatenated sequence of all 3 regions for females and males separately and for the whole data set with a computer program we wrote with S language. To estimate the 95% and 99% confidence intervals of these indices under the null model with the recombination rate estimated from the data by 4-gamate test (Hudson and Kaplan 1985), we conducted coalescent simulation using DnaSP (Munte et al. 2005). We estimated the recombination rate for each region separately and averaged these rates for the concatenated sequence. Because of high recombination frequency between the regions, the tests for the concatenated sequence are still conservative. To test the differences in D and F* values between females and males, we repeated the randomization protocol. The procedure for randomization was the same as that described above. The process of randomization was repeated 1000 times.
All the randomization tests were performed with statistical software R version 2.3 with programs written in S language. All the programs are available on request.
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Results |
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We surveyed sequence variation in 2.5 kb of total sequence for 4 chemoreceptor genes on 100 X chromosomes each from wild-caught female and male D. melanogaster. The sliding-window plot revealed relatively high nucleotide diversity at Or10a and at an intergenic region between Gr10a and Or10a; however, the pattern of nucleotide diversity was similar between females and males (Figure 3). Both
and 
values were relatively high at noncoding regions and silent sites in Gr5a and the Gr10a–Or10a region but uniformly low at replacement sites, regardless of sex (Table 1). The numbers of variable sites were similar between females and males when considering all variable sites in noncoding and coding regions (Table 2). In contrast, greater numbers of sex-specific singletons and doubletons were present in females than in males (Table 2). On the basis of genome information for related species Drosophila yakuba, D. simulans, and Drosophila sechellia, the rarer nucleotides at these sex-specific rare polymorphism sites appear to be derivatives. This difference in the number of sex-specifc singletons and doubletons between females and males was statistically significant (P = 0.022).
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LD values for common variable sites are shown separately for females and males in Figure 4. Trinucleotide segregating sites, which were relatively rare in our samples as well as rare polymorphisms, were excluded from this analysis. Relatively strong LD was observed between sites in Or10a and an intergenic region between Gr10a and Or10a; however, the general pattern of LD was similar between females and males. The average r2 value was 0.0719 for females and 0.0732 for males. The randomization test revealed that the average of r2 did not differ significantly between females and males (P = 0.84).
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Tajima's D and Fu and Li's F* detected significant departure from the neutrality at Gr5a in females and at Gr5a and the Gr10a–Or10a region in males, whereas Tajima's D detected significant departure from the neutrality at Gr5a and the Gr10a–Or10a region and Fu and Li's F* did at Gr5a in the whole data set (Table 3). When all regions were concatenated, significant departures from the neutrality were detected in females, males, and the whole data set by Tajima's D but only in males by Fu and Li's F* (Table 3). The differences in D and F* values between females and males were significant only at Gr8a when calculated by Fu and Li's F* (Table 3, column "randomization").
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Discussion |
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Although the Gr5a region and the region spanning Gr10a to Or10a showed relatively high nucleotide diversity and sites in Or10a and an intergenic region between Gr10a and Or10a showed relatively strong LD in both females and males, the general pattern of nucleotide diversity and LD was similar between females and males. In contrast, X chromosomes from males harbored a significantly lower number of rare polymorphisms than did those from females. The Tajima's D and Fu and Li's F* statistics were generally positively biased. For the concatenated sequence data, Tajima's D departed significantly from the expected neutrality in females, males, and the whole data set, whereas Fu and Li's F* value differed only in males.
The observed difference in the number of sex-specific rare polymorphisms was clearly too large to be explained by de novo mutations in germ cells of the wild-caught females and males (Drake et al. 1998). The paucity of rare polymorphisms in males can be explained by purifying selection against such variations. In contrast, a general selective explanation for the positive F* and D values (Table 3) is balancing selection and therefore contradicts the above explanation. This contradiction may be due to a composite and nonequilibrium nature of frequency spectrum of mutations. Demographic events in the past and the present profoundly influence these statistics. A recent moderate population bottleneck, for example, causes a deficit of rare polymorphisms, yielding positive F* and D values (Tajima 1989; Depaulis et al. 2003). In contrast to African D. melanogaster populations, non-African D. melanogaster populations often show haplotype dimorphism and significant deviations of Tajima's D from the neutral equilibrium expectation, suggesting a bottleneck or series of bottlenecks during and after out-of-Africa colonization or admixture of 2 divergent populations having experienced a bottleneck (Begun and Aquadro 1995; Langley et al. 2000; Teeter et al. 2000; Baudry et al. 2004). In these studies, Tajima's D deviated both positively and negatively from the neutrality. It is likely that the Japanese populations are not in equilibrium and that the demographic history produced the positive deviations of the D and F* values from the neutrality. Thus, the generally larger positive deviation of neutrality statistics in males than in females observed in the present study is explained by stronger purifying selection in males.
In sum, the findings obtained in this study suggest that some rare polymorphisms on the X chromosome in females are deleterious recessive polymorphisms that would be removed by stronger purifying selection when transferred to hemizygous males. Here, we assume a lack of sex-biased function and any sex-specific bias in selection intensity. On the other hand, there is significant sex-biased expression in the Drosophila transcriptome (Jin et al. 2001; Arbeitman et al. 2002; Parisi et al. 2003; Ranz et al. 2003). However, although slightly higher expression is reported in ovaries than in testes for Gr5a (Parisi et al. 2003), any sex-biased function is not known for the present 4 chemosensory receptor genes which are thought to functions in sensory neurons in larvae and adults. Indeed, there is no sex difference in phenotypes of Gr5a mutants (Tanimura et al. 1982; Dahanukar et al. 2001). In sum, there is no evidence for female-specific function for these genes, and they are likely exposed to stronger selection in hemizygous males than in females.
Transmission pattern of X chromosome might influence the relative abundance of sex-specific rare polymorphisms. In D. melanogaster, a female inherits her X chromosomes from both her female and male parents, whereas a male inherits his X chromosome only from his female parent. If purifying selection acts on X chromosomes mainly in males, X chromosomes of males with fewer rare deleterious polymorphisms after selection are transmitted only to females in the next generation. On the other hand, X chromosomes of females could bear more rare deleterious polymorphisms and are transmitted to both females and males. As a result, the number of rare polymorphisms on X chromosomes before selection in the next generation would be, on average, smaller in females than in males, counteracting the effect of purifying selection. The observed difference in the number of rare polymorphisms may, therefore, lead to an underestimation but not an overestimation of the effect of selection in the generation under consideration. In this sense, the present test for detecting current selection is conservative.
Selection that makes large differences in the number of sex-specific rare polymorphisms (i.e., 1 in males and 13 in females) should be strong. Mutations in the gustatory and olfactory receptor genes analyzed in the present study could negatively affect foraging behavior and could be selected against. Rollmann et al. (2006) reported that the gustatory receptor gene Gr5a in D. melanogaster also has pleiotropic fitness effects. They assessed the effect of a P-element insertion in the flanking region of Gr5a and found that the region also influences fitness traits such as selective nutrient intake, life span, and resistance to starvation and heat stress. Mutations in the region appear to interact epistatically with downstream components of the insulin signaling pathway, which has been implicated in regulation of longevity in Caenorhabditis elegans (Alcedo and Kenyon 2004) and D. melanogaster (Clancy et al. 2001; Hwangbo et al. 2004). If, in general, gustatory and olfactory receptor genes have such pleiotropic fitness effect, combined with the defects in foraging behavior, deleterious mutations in these genes could have significant effects on fitness, suggesting the possibility of strong purifying selection. However, we have no information regarding whether the sex-specific rare polymorphisms observed on X chromosomes from females really have deleterious effects in the hemizygous and homozygous states. Foraging behavior or other fitness traits should be compared between male flies with or without these sex-specific rare polymorphisms to evaluate their fitness effects.
On the other hand, the intensity of selection involved might be weaker than the observed difference indicated. If a truncation selection acts on clusters of these rare polymorphisms, the genetic load due to the deleterious mutations could be smaller than that when selection acts on each polymorphism independently (Kimura and Maruyama 1966; Crow and Kimura 1979; Kondrashov 1988). Indeed, the variance of the number of rare polymorphisms on the X chromosomes from females was greater than predicted from the Poisson distribution (F-test, P < 0.001), indicating that a subset of X chromosomes harbored an unexpectedly large number of rare polymorphisms, in other words, formed clusters. In addition, strong purifying selection may act not in every generation but only once in several generations. In previous research, we observed stronger degree of LD for Gr and Or genes in a spring population than in an autumn population (Takano-Shimizu et al. 2004), which might suggest the strong selection only in winter. Under this hypothesis, selection that accounts for the observed difference in the number of sex-specific rare polymorphisms does not necessarily lead to ultimate loss of genetic variation in the population. Seasonal change in selection intensity can be tested by comparing the number of rare polymorphisms between X chromosomes from female and male flies collected in autumn, in which we would expect a smaller difference than that obtained in the present study.
Several other factors might also contribute to the lower number of sex-specific polymorphisms on male X chromosomes than on female X chromosomes, although they are not mutually exclusive and to the selection-based explanation. One possibility is that the banana trap we used to collect wild D. melanogaster did not collect flies randomly from a local population, but instead selectively collected flies with fewer deleterious polymorphisms in the Gr and Or loci. If selection due to the banana trap is much stronger than the actual natural selection, it would reduce the number of sex-specific slightly deleterious polymorphisms detected on X chromosomes from hemizygous males, leading to an overestimation of natural selection. It is also possible that the effective range of the banana trap was somehow different for female and male flies. Because a larger number of rare polymorphisms are expected from samples consisting of flies from larger areas, the observed difference in the number of sex-specific rare alleles could be due to a larger effective range of the banana trap for females than males. This kind of fly sampling may also affect the amount of LD between common polymorphisms. If we collected closely related male flies due to sampling from a smaller area, we would expect a deficit of rare variants and stronger LD in males. However, we found no difference in the average r2 value between female and male X chromosomes. Therefore, there is little evidence to support this hypothesis. Although we cannot completely exclude population structure and sampling artifacts as factors influencing the present data, the observed pattern is likely to result from stronger purifying selection on X chromosomes in males.
The enhanced purifying selection against X chromosome variants is consistent with a previous report that the replacement-to-synonymous ratios for rare polymorphisms are much smaller for X-linked loci than for autosomal loci (0.06 vs. 0.63 in Fay et al. [2002]). Recently, based on the data of 337 genes, Connallon (2007) reported that the ratio of the number of singletons to that of nonsingletons at synonymous sites is significantly larger for the X-linked genes than for the autosomal genes in African populations (see Table 2 in Connallon [2007]). We cannot directly compare their numbers of rare polymorphisms without knowing the relative mutation rates for these X and autosomal genes and, therefore, nor say whether there is truly an excess of rare polymorphisms or a deficit of common polymorphisms. In the former case, the X-linked genes may be under weaker purifying selection than the autosomal ones in females. Alternatively, the stronger purifying selection on the X-linked genes can be suggested for the latter case. Replacement polymorphisms do not show any difference between the X and autosomal genes (Connallon 2007). This could be due to the very small sample sizes (5 or more). The magnitude of selection against replacement variants is generally expected to be larger than that against synonymous variants. Most deleterious replacement variants are present in very low frequency and then we likely failed to detect most of such variants.
In the faster-X hypothesis, more efficient fixation of advantageous mutations in hemizygous male is assumed as a mechanism of accelerated X chromosome evolution (Charlesworth et al. 1987). Although whether positive selection acts more efficiently on X-linked loci than on autosomal loci is still controversial, a higher Ka/Ks ratio for X-linked loci than autosomal loci has been observed in several studies of D. melanogaster (Thornton and Long 2002, 2004; Counterman et al. 2004), suggesting stronger positive selection on the X chromosome than on the autosomes. On the other hand, our present results indicate that a fraction of new mutations are removed in hemizygous males, suggesting that hemizygosity of the X chromosome also enhances the efficiency of purifying selection.
Comparison of the polymorphisms on X chromosomes from females and males, in principle, could reveal natural selection presently acting on the X chromosome, providing a novel heuristic approach to identify sites targeted by selection. This approach can be applied to any organism with heterogametic sex and to any genes on a sex chromosome. The approach is especially useful for analyzing between-locus interactions for organisms for which mutant and deficiency screenings in the laboratory are very difficult. Assessment of the impact of current natural selection and identification of target sites would further our understanding of how natural selection operates in natural populations.
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Funding |
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The Mitsubishi Foundation to T.T.-S.; Grant-in-Aid for Scientific Research (C) to T.T.-S. (#17570087); and National Institute of Genetics Cooperative Research Program to M.I. and T.T.-S. (#2006-17).
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Acknowledgments |
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We thank Kanna Takeshita, Yuriko Ishii, and Kimiko Suzuki for technical assistance and Shigeo Hayashi and Yasushi Hiromi for their support. Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession numbers AB283045 [GenBank] –AB284044.
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Footnotes |
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Corresponding Editor: James Thompson
Received October 9, 2007
Revised July 21, 2008
Accepted August 18, 2008
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