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Higher Frequency of Concerted Evolutionary Events in Rodents Than in Man at the Polyubiquitin Gene VNTR Locus

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Higher Frequency of Concerted Evolutionary Events in Rodents Than in Man at the Polyubiquitin Gene VNTR Locus Copyright © 1998 by the Genetics Society of America Higher Frequency of Concerted Evolutionary Events in Rodents Than in Man at the Polyubiquitin Gene VNTR Locus Mitsuru Nenoi,* Kazuei Mita,† Sachiko Ichimura,* and Akihiro Kawano‡ *Division of Biology and Oncology, †Genome Research Group and ‡Laboratory of Animal and Plant Sciences, National Institute of Radiological Sciences, Inage-ku, Chiba 263 Japan Manuscript received July 28, 1997 Accepted for publication October 24, 1997 ABSTRACT The polyubiquitin gene is an evolutionarily conserved eukaryotic gene, encoding tandemly repeated multiple ubiquitins, and is considered to be subject to concerted evolution. Here, we present the nucle- otide sequences of new alleles of the polyubiquitin gene UbC in humans and CHUB2 in Chinese hamster, which encode a different number of ubiquitin units from those of previously reported genes. And we ana- lyze the concerted evolution of these genes on the basis of their orthologous relationship. That the mean of the synonymous sequence difference Ks, which is defined as the number of synonymous substitution rel- ative to the total number of synonymous sites, within the UbC and CHUB2 genes (0.192 6 0.096) is signifi- cantly less than Ks between these genes (0.602 6 0.057) provides direct evidence for concerted evolution. Moreover, it also appears that concerted evolutionary events have been much more frequent in CHUB2 than in UbC, because Ks within CHUB2 (0.022 6 0.018) is much less than that within UbC (0.362 6 0.192). By a numerical simulation, postulating that the major mechanism of concerted evolution in polyubiquitin genes is unequal crossing over, we estimated the frequency of concerted evolutionary events of CHUB2 at 3.3 3 1025 per year and that of UbC at no more than 5.0 3 1027 per year. BIQUITIN is a highly conserved small protein coding nine units, and the other less frequent alleles U of 76 amino acids functioning in the selective encoding eight or seven units (Baker and Board proteolysis of a variety of cellular proteins at the 26S 1989). The nucleotide sequence GNNGTGGG, which proteasome (Hochstrasser 1996; Ciechanover and has been found to be the consensus marker sequence Schwartz 1994). In addition, ubiquitin has been for a variable number of tandem repeat (VNTR) loci in shown to function in proteasome action-independent humans (Nakamura et al. 1988), is preserved at the 39 processes such as DNA repair (Bregman et al. 1996), end of every ubiquitin-coding unit of the UbC. We have endocytosis of cell surface proteins (Hicke and Riez- actually observed that the UbC gene alleles of HeLa man 1996), and NFkB signal transduction (Chen et al. cells (Nenoi et al. 1996) as well as the Chinese hamster 1996). In humans, ubiquitin is encoded by a multiple polyubiquitin gene CHUB2 of V79 fibroblasts (Nenoi et gene family composed of UbA52, UbA80, UbB, and UbC al. 1994) are heterogeneous in the repeat number of (Baker and Board 1991, 1987; Wiborg et al. 1985). the ubiquitin units. The UbB and UbC genes, located on chromosome 17 It has been suggested that the polyubiquitin genes (17p11.1-17p12) (Webb et al. 1990) and chromosome may show strong evidence of concerted evolution 12 (12q24.3) (Board et al. 1992), respectively, are (Sharp and Li 1987; Tan et al. 1993; Keeling and termed polyubiquitin genes because they encode tan- Doolittle 1995; Vrana and Wheeler 1996). This is demly repeated multiple ubiquitins with no interven- consistent with observations of a high variability in the ing spacer. The polyubiquitin genes are conserved also number of the ubiquitin-coding units in the UbC and in rodents, and we previously isolated and sequenced CHUB2 genes because unequal crossing over is be- the Chinese hamster polyubiquitin genes, CHUB1 and lieved to be one of the major mechanisms for con- CHUB2, which are the counterparts of the human UbB certed evolution (Dover 1982; Darnell et al. 1990). A and UbC, respectively (Nenoi et al. 1992; Nenoi et al. greater degree of homology between repeat units 1994). Due to unequal crossing over, the number of within a species as compared to orthologous repeat ubiquitin units encoded by the UbC gene is variable units in different species is a diagnostic of concerted among individuals, with the most frequent allele en- evolution. However, in the case of the polyubiquitin gene, data have not been available for all loci in each species, and it has not been clear whether the loci com- pared across species are orthologues or paralogues. Corresponding author: Dr. Mitsuru Nenoi, Division of Biology and Oncology, National Institute of Radiological Sciences, 9-1, Anagawa- In this report, we will analyze the unequal crossover 4-chome, Inage-ku, Chiba-shi 263 Japan. E-mail: [email protected] events that are thought to have occurred on the human Genetics 148: 867–876 (February, 1998) 868 M. Nenoi et al. UbC gene and the Chinese hamster CHUB2 gene, and tionary change of Ks between the ubiquitin-coding units within we will analyze the concerted evolution of these genes a given polyubiquitin gene after the divergence of human and rodents. Let K (i,j;t) be the synonymous sequence difference on the basis of their orthologous relationship. It will be s between the i-th and j-th ubiquitin unit of a given polyubiq- proposed that the UbC gene that encodes nine ubiqui- uitin gene at a time t. By definition, tins was recently generated by an unequal crossover ()= () % % event between a site in the seventh ubiquitin-coding Ks j, i; t Ksi, j; t 1 i, j N () unit and the homologous site in the sixth unit of the Ks i, i; t = 0 1 % i % N UbC gene that encodes eight ubiquitins. We will also where N is the number of ubiquitin units encoded by the show a much higher homology between the ubiquitin- polyubiquitin gene at the time of t. Random numbers were coding units within the CHUB2 gene than within the generated to provide the dates of the unequal crossover UbC gene, which could be explained by a higher fre- events. The event type (unit-duplication or unit-deletion) was quency of unequal crossover events during the evolu- also determined randomly under the constraint that the unit tion of the CHUB2. number is kept between one and the maximum number, which was set at 20 in this study, and that the final unit num- ber reaches that of the actual genes after the simulation. Dur- ing a time interval, dt, between the adjacent events, every syn- MATERIALS AND METHODS onymous sequence difference increases by vdt, where v is the Isolation and sequencing of the polyubiquitin genes: evolutionary rate of synonymous substitution. Then, HeLa cells and V79 Chinese hamster lung fibroblasts were K ()i, j; t + δt = K()i, j; t + vδt 1 % i, j % N cultured in Eagle’s MEM (Nissui, Tokyo, Japan) supple- s s mented with 10% FBS (GIBCO BRL, Rockville, MD). Fresh If a unit-duplication event occurs at the n-th unit at this mo- thymus from a Chinese hamster was generously provided by ment, Dr. Mitsuhiro Numata (National Institute of Health, Japan). The method for isolation of the polyubiquitin genes has been K ()i, j; t + δt =K()i, j; t + δt 1 % i, j % n described (Nenoi et al. 1996). Briefly, the genomic DNA was s s ()+ δ =()– + δ % % + % % + extracted from cell suspension, and the DNA fragment con- Ks i, j; t t Ksi, j 1; t t 1 in, n 1 j N 1 ()δ ()δ taining the whole ubiquitin-coding region was amplified by Ks i, j; t + t =Ksi– 1, j; t + t n+ 1 % i % N + 1, 1 % j % n PCR using LA polymerase (TAKARA, Otsu, Japan). Prim- Taq K ()i, j; t + δt =K()i– 1, j – 1; t + δt n+ 1 % i, j % N + 1 ers specific to the 59 and 39 flanking region of the UbC gene s s were designed on the basis of the reported nucleotide se- On the other hand, if a unit-deletion event occurs at the n-th Wiborg Nenoi quences ( et al. 1985; et al. 1996); P.Hu1: 59- unit, TTGGGCAGTGCACCCGTACCTTTGG-39, P.Hu2: 59-GTGC AATGAAATTTGTTGAAACCTTAAAAGGGG-39, and of the K ()i, j; t + δt =K()i, j; t + δt 1 % i, j % n – 1 CHUB2 gene (Nenoi et al. 1994); P.CH1: 59-CCACGAATAT s s ()δ ()δ TTGTCATTCCTGACCTG-39, P.CH2: 59-GCTAAAACGAGAT Ks i, j; t + t =Ksi, j ++1; t t 1 % i % n – 1, n % j % N – 1 9 ()δ ()δ CCAACACCTTTGGG-3 (indicated in Figure 2). A series of Ks i, j; t + t =Ksi++1, j; t t n % i % N – 1, 1 % j % n – 1 deletion mutants was constructed by partially digesting the K ()i, j; t + δt =K()i++1, j 1; t +δt n % i, j % N – 1 PCR products either with PvuII (for UbC) or with BglII (for s s CHUB2), followed by subcloning in the pUC18 and then se- These calculations were repeated for the time from the man- quencing with an automated DNA sequencer (model 373A; rodent split (t 5 0) until the present (t 5 1.2 3 108). Applied Biosystems, Foster City, CA). The sequence data presented in this article have been sub- Sequence analysis: The homology analysis between every mitted to the DDBJ/EMBL/GenBank databases under acces- pair of ubiquitin-coding units in the UbC and CHUB2 was car- sion numbers AB003730, AB003731, and AB003732. ried out by evaluating the synonymous sequence difference per site, Ks, which is defined as the number of synonymous substitution relative to the total number of synonymous sites RESULTS AND DISCUSSION Miyata Yasunaga ( and 1980).
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