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. 1995 Feb;139(2):921–939. doi: 10.1093/genetics/139.2.921

Structure and Evolution of Genes Encoding Polyubiquitin and Ubiquitin-like Proteins in Arabidopsis Thaliana Ecotype Columbia

J Callis 1, T Carpenter 1, C W Sun 1, R D Vierstra 1
PMCID: PMC1206391  PMID: 7713442

Abstract

The Arabidopsis thaliana ecotype Columbia ubiquitin gene family consists of 14 members that can be divided into three types of ubiquitin genes; polyubiquitin genes, ubiquitin-like genes and ubiquitin extension genes. The isolation and characterization of eight ubiquitin sequences, consisting of four polyubiquitin genes and four ubiquitin-like genes, are described here, and their relationships to each other and to previously identified Arabidopsis ubiquitin genes were analyzed. The polyubiquitin genes, UBQ3, UBQ10, UBQ11 and UBQ14, contain tandem repeats of the 228-bp ubiquitin coding region. Together with a previously described polyubiquitin gene, UBQ4, they differ in synonymous substitutions, number of ubiquitin coding regions, number and nature of nonubiquitin C-terminal amino acid(s) and chromosomal location, dividing into two subtypes; the UBQ3/UBQ4 and UBQ10/UBQ11/UBQ14 subtypes. Ubiquitin-like genes, UBQ7, UBQ8, UBQ9 and UBQ12, also contain tandem repeats of the ubiquitin coding region, but at least one repeat per gene encodes a protein with amino acid substitutions. Nucleotide comparisons, K(s) value determinations and neighbor-joining analyses were employed to determine intra- and intergenic relationships. In general, the rate of synonymous substitution is too high to discern related repeats. Specific exceptions provide insight into gene relationships. The observed nucleotide relationships are consistent with previously described models involving gene duplications followed by both unequal crossing-over and gene conversion events.

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Selected References

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  1. Agarwal M. L., Cullis C. A. The ubiquitin-encoding multigene family of flax, Linum usitatissimum. Gene. 1991 Mar 1;99(1):69–75. doi: 10.1016/0378-1119(91)90035-a. [DOI] [PubMed] [Google Scholar]
  2. Allison L. A., Moyle M., Shales M., Ingles C. J. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell. 1985 Sep;42(2):599–610. doi: 10.1016/0092-8674(85)90117-5. [DOI] [PubMed] [Google Scholar]
  3. Athma P., Peterson T. Ac induces homologous recombination at the maize P locus. Genetics. 1991 May;128(1):163–173. doi: 10.1093/genetics/128.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker R. T., Board P. G. Nucleotide sequence of a human ubiquitin Ub B processed pseudogene. Nucleic Acids Res. 1987 May 26;15(10):4352–4352. doi: 10.1093/nar/15.10.4352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baker R. T., Board P. G. Unequal crossover generates variation in ubiquitin coding unit number at the human UbC polyubiquitin locus. Am J Hum Genet. 1989 Apr;44(4):534–542. [PMC free article] [PubMed] [Google Scholar]
  6. Baker R. T., Tobias J. W., Varshavsky A. Ubiquitin-specific proteases of Saccharomyces cerevisiae. Cloning of UBP2 and UBP3, and functional analysis of the UBP gene family. J Biol Chem. 1992 Nov 15;267(32):23364–23375. [PubMed] [Google Scholar]
  7. Binet M. N., Steinmetz A., Tessier L. H. The primary structure of sunflower (Helianthus annuus) ubiquitin. Nucleic Acids Res. 1989 Mar 11;17(5):2119–2119. doi: 10.1093/nar/17.5.2119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Binet M. N., Weil J. H., Tessier L. H. Structure and expression of sunflower ubiquitin genes. Plant Mol Biol. 1991 Sep;17(3):395–407. doi: 10.1007/BF00040634. [DOI] [PubMed] [Google Scholar]
  9. Bond U., Schlesinger M. J. Ubiquitin is a heat shock protein in chicken embryo fibroblasts. Mol Cell Biol. 1985 May;5(5):949–956. doi: 10.1128/mcb.5.5.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Callis J., Pollmann L., Shanklin J., Wettern M., Vierstra R. D. Sequence of a cDNA from Chlamydomonas reinhardii encoding a ubiquitin 52 amino acid extension protein. Nucleic Acids Res. 1989 Oct 25;17(20):8377–8377. doi: 10.1093/nar/17.20.8377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Callis J., Raasch J. A., Vierstra R. D. Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem. 1990 Jul 25;265(21):12486–12493. [PubMed] [Google Scholar]
  12. Christensen A. H., Sharrock R. A., Quail P. H. Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol. 1992 Feb;18(4):675–689. doi: 10.1007/BF00020010. [DOI] [PubMed] [Google Scholar]
  13. Cowland J. B., Wiborg O., Vuust J. Human ubiquitin genes: one member of the UbB gene subfamily is a tetrameric non-processed pseudogene. FEBS Lett. 1988 Apr 11;231(1):187–191. doi: 10.1016/0014-5793(88)80728-2. [DOI] [PubMed] [Google Scholar]
  14. Das O. P., Levi-Minzi S., Koury M., Benner M., Messing J. A somatic gene rearrangement contributing to genetic diversity in maize. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7809–7813. doi: 10.1073/pnas.87.20.7809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  17. Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. doi: 10.1146/annurev.ge.22.120188.002513. [DOI] [PubMed] [Google Scholar]
  18. Finley D., Bartel B., Varshavsky A. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature. 1989 Mar 30;338(6214):394–401. doi: 10.1038/338394a0. [DOI] [PubMed] [Google Scholar]
  19. Finley D., Chau V. Ubiquitination. Annu Rev Cell Biol. 1991;7:25–69. doi: 10.1146/annurev.cb.07.110191.000325. [DOI] [PubMed] [Google Scholar]
  20. Garbarino J. E., Rockhold D. R., Belknap W. R. Expression of stress-responsive ubiquitin genes in potato tubers. Plant Mol Biol. 1992 Oct;20(2):235–244. doi: 10.1007/BF00014491. [DOI] [PubMed] [Google Scholar]
  21. Genschik P., Parmentier Y., Durr A., Marbach J., Criqui M. C., Jamet E., Fleck J. Ubiquitin genes are differentially regulated in protoplast-derived cultures of Nicotiana sylvestris and in response to various stresses. Plant Mol Biol. 1992 Dec;20(5):897–910. doi: 10.1007/BF00027161. [DOI] [PubMed] [Google Scholar]
  22. Guarino L. A. Identification of a viral gene encoding a ubiquitin-like protein. Proc Natl Acad Sci U S A. 1990 Jan;87(1):409–413. doi: 10.1073/pnas.87.1.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Haas A. L., Ahrens P., Bright P. M., Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J Biol Chem. 1987 Aug 15;262(23):11315–11323. [PubMed] [Google Scholar]
  24. Hanley B. A., Schuler M. A. Plant intron sequences: evidence for distinct groups of introns. Nucleic Acids Res. 1988 Jul 25;16(14B):7159–7176. doi: 10.1093/nar/16.14.7159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hatfield P. M., Callis J., Vierstra R. D. Cloning of ubiquitin activating enzyme from wheat and expression of a functional protein in Escherichia coli. J Biol Chem. 1990 Sep 15;265(26):15813–15817. [PubMed] [Google Scholar]
  26. Heidecker G., Chaudhuri S., Messing J. Highly clustered zein gene sequences reveal evolutionary history of the multigene family. Genomics. 1991 Jul;10(3):719–732. doi: 10.1016/0888-7543(91)90456-o. [DOI] [PubMed] [Google Scholar]
  27. Hershko A., Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761–807. doi: 10.1146/annurev.bi.61.070192.003553. [DOI] [PubMed] [Google Scholar]
  28. Jeffreys A. J., Harris S. Processes of gene duplication. Nature. 1982 Mar 4;296(5852):9–10. doi: 10.1038/296009a0. [DOI] [PubMed] [Google Scholar]
  29. Jones D., Candido E. P. Novel ubiquitin-like ribosomal protein fusion genes from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Biol Chem. 1993 Sep 15;268(26):19545–19551. [PubMed] [Google Scholar]
  30. Jonnalagadda S., Butt T. R., Monia B. P., Mirabelli C. K., Gotlib L., Ecker D. J., Crooke S. T. Multiple (alpha-NH-ubiquitin)protein endoproteases in cells. J Biol Chem. 1989 Jun 25;264(18):10637–10642. [PubMed] [Google Scholar]
  31. Kawalleck P., Somssich I. E., Feldbrügge M., Hahlbrock K., Weisshaar B. Polyubiquitin gene expression and structural properties of the ubi4-2 gene in Petroselinum crispum. Plant Mol Biol. 1993 Feb;21(4):673–684. doi: 10.1007/BF00014550. [DOI] [PubMed] [Google Scholar]
  32. Kridl J. C., Vieira J., Rubenstein I., Messing J. Nucleotide sequence analysis of a zein genomic clone with a short open reading frame. Gene. 1984 Apr;28(1):113–118. doi: 10.1016/0378-1119(84)90093-3. [DOI] [PubMed] [Google Scholar]
  33. Lander E. S., Green P., Abrahamson J., Barlow A., Daly M. J., Lincoln S. E., Newberg L. A., Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. doi: 10.1016/0888-7543(87)90010-3. [DOI] [PubMed] [Google Scholar]
  34. Lassner M., Dvorak J. Preferential homogenization between adjacent and alternate subrepeats in wheat rDNA. Nucleic Acids Res. 1986 Jul 11;14(13):5499–5512. doi: 10.1093/nar/14.13.5499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lyons K. M., Stein J. H., Smithies O. Length polymorphisms in human proline-rich protein genes generated by intragenic unequal crossing over. Genetics. 1988 Sep;120(1):267–278. doi: 10.1093/genetics/120.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Maeda N., Smithies O. The evolution of multigene families: human haptoglobin genes. Annu Rev Genet. 1986;20:81–108. doi: 10.1146/annurev.ge.20.120186.000501. [DOI] [PubMed] [Google Scholar]
  37. Mayer A. N., Wilkinson K. D. Detection, resolution, and nomenclature of multiple ubiquitin carboxyl-terminal esterases from bovine calf thymus. Biochemistry. 1989 Jan 10;28(1):166–172. doi: 10.1021/bi00427a024. [DOI] [PubMed] [Google Scholar]
  38. Metzenberg R. L., Stevens J. N., Selker E. U., Morzycka-Wroblewska E. Identification and chromosomal distribution of 5S rRNA genes in Neurospora crassa. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2067–2071. doi: 10.1073/pnas.82.7.2067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ohmachi T., Giorda R., Shaw D. R., Ennis H. L. Molecular organization of developmentally regulated Dictyostelium discoideum ubiquitin cDNAs. Biochemistry. 1989 Jun 13;28(12):5226–5231. doi: 10.1021/bi00438a046. [DOI] [PubMed] [Google Scholar]
  40. Pedersen K., Devereux J., Wilson D. R., Sheldon E., Larkins B. A. Cloning and sequence analysis reveal structural variation among related zein genes in maize. Cell. 1982 Jul;29(3):1015–1026. doi: 10.1016/0092-8674(82)90465-2. [DOI] [PubMed] [Google Scholar]
  41. Pichersky E., Bernatzky R., Tanksley S. D., Breidenbach R. B., Kausch A. P., Cashmore A. R. Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (tomato). Gene. 1985;40(2-3):247–258. doi: 10.1016/0378-1119(85)90047-2. [DOI] [PubMed] [Google Scholar]
  42. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  43. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  44. Sanders P. R., Winter J. A., Barnason A. R., Rogers S. G., Fraley R. T. Comparison of cauliflower mosaic virus 35S and nopaline synthase promoters in transgenic plants. Nucleic Acids Res. 1987 Feb 25;15(4):1543–1558. doi: 10.1093/nar/15.4.1543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sugita M., Gruissem W. Developmental, organ-specific, and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7104–7108. doi: 10.1073/pnas.84.20.7104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sugita M., Manzara T., Pichersky E., Cashmore A., Gruissem W. Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato. Mol Gen Genet. 1987 Sep;209(2):247–256. doi: 10.1007/BF00329650. [DOI] [PubMed] [Google Scholar]
  48. Sun C. W., Callis J. Recent stable insertion of mitochondrial DNA into an Arabidopsis polyubiquitin gene by nonhomologous recombination. Plant Cell. 1993 Jan;5(1):97–107. doi: 10.1105/tpc.5.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tovar J., Lichtenstein C. Somatic and Meiotic Chromosomal Recombination between Inverted Duplications in Transgenic Tobacco Plants. Plant Cell. 1992 Mar;4(3):319–332. doi: 10.1105/tpc.4.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]
  51. Wandelt C., Feix G. Sequence of a 21 kd zein gene from maize containing an in-frame stop codon. Nucleic Acids Res. 1989 Mar 25;17(6):2354–2354. doi: 10.1093/nar/17.6.2354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Watkins J. F., Sung P., Prakash L., Prakash S. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol Cell Biol. 1993 Dec;13(12):7757–7765. doi: 10.1128/mcb.13.12.7757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wiborg O., Pedersen M. S., Wind A., Berglund L. E., Marcker K. A., Vuust J. The human ubiquitin multigene family: some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J. 1985 Mar;4(3):755–759. doi: 10.1002/j.1460-2075.1985.tb03693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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