Abstract
Ubiquitin is a highly conserved protein, and is encoded by a multigene family among eukaryote species. The polyubiquitin genes, UbB and UbC, comprise tandem multiple ubiquitin coding units without a spacer region or intron. We determined nucleotide sequences for the UbB and UbC of human, chimpanzee, gorilla, and orangutan. The ubiquitin repeat number of UbB was constant (3) in human and great apes, while that of UbC varied: 6 to 11 for human, 10 to 12 for chimpanzee, 8 for gorilla, and 10 for orangutan. The heterogeneity of the repeat number within closely related hominoid species suggests that a lineage-specific unequal crossover and/or gene duplication occurred. A marked homogenization of UbC occurred in gorilla with a low level of synonymous difference (p s ). The homogenization of UbC also occurred in chimpanzee and less strikingly in human. The first and last ubiquitin coding units of UbC were clustered independently between species, and less affected by homogenization during the hominoid evolution. Therefore, the homogenization of ubiquitin coding units is likely due to an unequal crossing-over inside the ubiquitin units. The lineage-specific homogenization of UbC among closely related species suggests that concerted evolution has a key role in the short-term evolution of UbC.
Similar content being viewed by others
References
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 3389–3402 Occurrence Handle9254694
F Apiou D Flagiello CB Cillo B Malfoy MF Poupon B Dutrillaux (1996) ArticleTitleFine mapping of human HOX gene clusters. Cytogenet Cell Genet 73 114–115 Occurrence Handle1:CAS:528:DyaK28XkvVarurc%3D Occurrence Handle8646877
WJ Bailey J Kim GP Wagner FH Ruddle (1997) ArticleTitlePhylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol Evol 14 843–853 Occurrence Handle1:CAS:528:DyaK2sXltVeisbw%3D Occurrence Handle9254922
RT Baker PG Board (1987) ArticleTitleThe human ubiquitin gene family: Structure of a gene and pseudogenes from the UbB subfamily. Nucleic Acids Res 15 443–463 Occurrence Handle1:CAS:528:DyaL2sXhvFSjtLg%3D Occurrence Handle3029682
RT Baker PG Board (1989) ArticleTitleUnequal crossover generates variation in ubiquitin coding unit number at the human UbC polyubiquitin locus. Am J Hum Genet 44 534–542 Occurrence Handle1:CAS:528:DyaL1MXit1Kns7o%3D Occurrence Handle2564731
RT Baker PG Board (1991) ArticleTitleThe human ubiquitin-52 amino acid fusion protein gene shares several structural features with mammalian ribosomal protein genes. Nucleic Acids Res 19 1035–1040 Occurrence Handle1:CAS:528:DyaK3MXlt1yrsr8%3D Occurrence Handle1850507
PG Board M Coggan RT Baker J Vuust GC Webb (1992) ArticleTitleLocalization of the human UBC polyubiquitin gene to chromosome band 12q24.3. Genomics 12 639–642 Occurrence Handle1:CAS:528:DyaK38Xit12ntr0%3D Occurrence Handle1315303
IL Gonzalez JE Sylvester (2001) ArticleTitleHuman rDNA: Evolutionary patterns within the genes and tandem arrays derived from multiple chromosomes. Genomics 73 255–263 Occurrence Handle10.1006/geno.2001.6540 Occurrence Handle1:CAS:528:DC%2BD3MXjtlGgsLY%3D Occurrence Handle11350117
M Kasahara M Hayashi K Tanaka H Inoko K Sugaya T Ikemura T Ishibashi (1996) ArticleTitleChromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. Proc Natl Acad Sci USA 93 9096–9101 Occurrence Handle10.1073/pnas.93.17.9096 Occurrence Handle1:CAS:528:DyaK28Xlt1Chsbc%3D Occurrence Handle8799160
S Kawamura N Saitou S Ueda (1992) ArticleTitleConcerted evolution of the primate immunoglobulin alpha-gene through gene conversion. J Biol Chem 267 7359–7367 Occurrence Handle1:CAS:528:DyaK38Xitlelsr4%3D Occurrence Handle1559979
PI Keeling WF Doolittle (1995) ArticleTitleConcerted evolution in protists: Recent homogenization of a polyubiquitin gene in Trichomonas vaginalis. J Mol Evol 41 556–562 Occurrence Handle1:CAS:528:DyaK2MXpsVKgtL8%3D Occurrence Handle7490769
M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111–120 Occurrence Handle7463489
T Kitano N Saitou (1999) ArticleTitleEvolution of the Rh blood group genes has experienced gene conversions and positive selection. J Mol Evol 49 615–626 Occurrence Handle1:CAS:528:DyaK1MXnsVajtr4%3D Occurrence Handle10552043
S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17 1244–1245 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241
WH Li (1997) Molecular evolution. Sinauer Associates Sunderland, MA
D Liao (1999) ArticleTitleConcerted evolution: Molecular mechanism and biological implications. Am J Hum Genet 64 24–30 Occurrence Handle1:CAS:528:DyaK1MXht1emu7k%3D Occurrence Handle9915939
PK Lund BM Moats-Staats JG Simmons E Hoyt AJ D’Ercole F Martin JJ Van Wyk (1985) ArticleTitleNucleotide sequence analysis of a cDNA encoding human ubiquitin reveals that ubiquitin is synthesized as a precursor. J Biol Chem 260 7609–7613 Occurrence Handle1:CAS:528:DyaL2MXltFOhuro%3D Occurrence Handle2581967
M Nei (1987) Molecular evolutionary genetics. Columbia University Press New York
M Nei IB Rogozin H Piontkivska (2000) ArticleTitlePurifying selection and birth-and-death evolution in the ubiquitin gene family. Proc Natl Acad Sci USA 97 10866–10871 Occurrence Handle10.1073/pnas.97.20.10866 Occurrence Handle1:CAS:528:DC%2BD3cXnt1ahs7o%3D Occurrence Handle11005860
M Nenoi K Mita S Ichimura IL Cartwright (1994) ArticleTitleNovel structure of a Chinese hamster polyubiquitin gene. Biochim Biophys Acta 1204 271–278 Occurrence Handle10.1016/0167-4838(94)90018-3 Occurrence Handle1:CAS:528:DyaK2cXlt1Kgtbw%3D Occurrence Handle8142469
M Nenoi K Mita S Ichimura IL Cartwright E Takahashi M Yamauchi H Tsuji (1996) ArticleTitleHeterogeneous structure of the polyubiquitin gene UbC of HeLa S3 cells. Gene 175 179–185 Occurrence Handle10.1016/0378-1119(96)00145-X Occurrence Handle1:CAS:528:DyaK28XmtlehtL4%3D Occurrence Handle8917096
M Nenoi K Mita S Ichimura A Kawano (1998) ArticleTitleHigher frequency of concerted evolutionary events in rodents than in man at the polyubiquitin gene VNTR locus. Genetics 148 867–876 Occurrence Handle1:CAS:528:DyaK1cXks1eisbc%3D Occurrence Handle9504932
M Nenoi S Ichimura K Mita (2000) ArticleTitleInterspecific comparison in the frequency of concerted evolution at the polyubiquitin gene locus. J Mol Evol 51 161–165 Occurrence Handle1:CAS:528:DC%2BD3cXmsVOrs7o%3D Occurrence Handle10948272
S Ohno (1970) Evolution by gene duplication. Springer-Verlag New York
E Pennisi (2001) ArticleTitleGenome duplications: The stuff of evolution? Science 294 2458–2460 Occurrence Handle10.1126/science.294.5551.2458 Occurrence Handle1:CAS:528:DC%2BD38XntVCr Occurrence Handle11752552
KL Redman M Rechsteiner (1989) ArticleTitleIdentification of the long ubiquitin extension as ribosomal protein S27a. Nature 338 438–440 Occurrence Handle10.1038/338438a0 Occurrence Handle1:CAS:528:DyaL1MXitVyjt7w%3D Occurrence Handle2538756
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
PM Sharp WH Li (1987) ArticleTitleUbiquitin genes as a paradigm of concerted evolution of tandem repeats. J Mol Evol 25 58–64 Occurrence Handle1:CAS:528:DyaL2sXksFenu7w%3D Occurrence Handle3041010
L Skrabanek KH Wolfe (1998) ArticleTitleEukaryote genome duplication—Where’s the evidence? Curr Opin Genet Dev 8 694–700
A Sidow (1996) ArticleTitleGen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 6 715–722 Occurrence Handle1:CAS:528:DyaK2sXhsVWjsw%3D%3D Occurrence Handle8994842
Y Tan ST Bishoff MA Riley (1993) ArticleTitleUbiquitins revisited: Further examples of within- and between-locus concerted evolution. Mol Phylogenet Evol 2 260–351
JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673–4680 Occurrence Handle7984417
PE Vrana WC Wheeler (1996) ArticleTitleMolecular evolution and phylogenetic utility of the polyubiquitin locus in mammals and higher vertebrates. Mol Phylogenet Evol 6 259–269 Occurrence Handle1:CAS:528:DyaK28XmvFOjtb8%3D Occurrence Handle8899727
GC Webb RT Baker K Fagan PG Board (1990) ArticleTitleLocalization of the human UbB polyubiquitin gene to chromosome band 17p11.l-17p12. Am J Hum Genet 46 308–315 Occurrence Handle1:CAS:528:DyaK3cXhsFaru7Y%3D Occurrence Handle2154095
O Wiborg MS Pedersen A Wind LE Berglund KA Marcker J Vuust (1985) ArticleTitleThe human ubiquitin multigene family: Some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J 4 755–759 Occurrence Handle1:CAS:528:DyaL28XivFKktw%3D%3D Occurrence Handle2988935
Acknowledgements
This work was supported in part by a Research for the Future Program Grant of The Japan Society for the Promotion of Science to I.I and Grants-in-Aid for Scientific Research on priority areas from the Ministry of Education, Culture, Sport, Science, and Technology of Japan to N.S. We thank Ms. Kozue Otaka for her technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tachikui, H., Saitou, N., Nakajima, T. et al. Lineage-Specific Homogenization of the Polyubiquitin Gene Among Human and Great Apes . J Mol Evol 57, 737–744 (2003). https://doi.org/10.1007/s00239-003-2532-4
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00239-003-2532-4