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Members of two gene families encoding ubiquitin-conjugating enzymes, AtUBC1-3 and AtUBC4-6, fromArabidopsis thaliana are differentially expressed

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Abstract

Covalent attachment of ubiquitin to other intracellular proteins is essential for many physiological processes in eukaryotes, including selective protein degradation. Selection of proteins for ubiquitin conjugation is accomplished, in part, by a group of enzymes designated E2s or ubiquitin-conjugating enzymes (UBCs). At least six types of E2s have been identified in the plantArabidopsis thaliana; each type is encoded by a small gene family. Previously, we described the isolation and characterization of two three-member gene families, designatedAtUBC1-3 andAtUBC4-6, encoding two of these E2 types. Here, we investigated the expression patterns, of theAtUBC1-3 andAtUBC4-6 genes by the histochemical analysis of transgenicArabidopsis containing the corresponding promoters fused to the β-glucuronidase-coding region. Staining patterns showed that these genes are active in many stages of development and some aspects of cell death, but are not induced by heat stress. Within the two gene families, individual members exhibited both overlapping and complementary expression patterns, indicating that at least one member of each gene family is expressed in most cell types and at most developmental stages. Different composite patterns of expression were observed between theAtUBC1-3 andAtUBC4-6 families, suggesting distinct biochemical and/or physiological functions for the encoded E2s inArabidopsis.

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References

  1. An G, Ebert PR, Mitra A, Ha SB: Binary vectors. In: Gelvin SB, Schilperoort RA (eds) Plant Molecular Biology Manual, pp. A3: 1–19. Kluwer Academic Publishers, Dordrecht, the Netherlands (1988).

    Google Scholar 

  2. Bachmair A, Becker F, Masterson V, Schell J: Pertubation of the ubiquitin system causes leaf curling, vascular tissue alterations, and necrotic lesions in a higher plant. EMBO J 9: 4543–4549 (1991).

    Google Scholar 

  3. Bartling D, Rehling P, Weiler EW: Functional expression and molecular characterization of AtUBC2–1, a novel ubiquitin-conjugating enzyme (E2) fromArabidopsis thaliana. Plant Mol Biol 23: 387–396 (1993).

    PubMed  Google Scholar 

  4. Britt AB, Chen J-J, Wykoff D, Mitchell D: A UV-sensitive mutant ofArabidopsis thaliana defective in repair of pyrimidine (6–4) pyrimidinone dimers. Science 261: 1571–1574 (1993).

    PubMed  Google Scholar 

  5. Burke TJ, Callis JA, Vierstra RD: Characterization of a polyubiquitin gene inArabidopsis thaliana. Mol Gen Genet 213: 435–443 (1988).

    PubMed  Google Scholar 

  6. Callis JA: Regulation of protein degradation. Plant Cell 7: 845–857 (1995).

    Article  PubMed  Google Scholar 

  7. Callis JA, Raasch JA, Vierstra RD: Ubiquitin extension proteins inArabidopsis thaliana: structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem 265: 12468–12493 (1990).

    Google Scholar 

  8. Christensen AH, Sharrock RA, Quail PH: Maize polyubiquitin genes, structure, thermal perturbation of expression, transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18: 675–689 (1992).

    PubMed  Google Scholar 

  9. Ciechanover A: The ubiquitin-proteasome proteolytic pathway. Cell 79: 13–21 (1994).

    Article  PubMed  Google Scholar 

  10. Collins BA, Reed PD, Rubinstein B: Ubiquitinated proteins in differentiating vascular tissue ofColeus blumei. Plant Physiol 102: 125 (1993).

    PubMed  Google Scholar 

  11. Cook WJ, Jeffrey LC, Sullivan ML, Vierstra RD: Three-dimensional structure of a ubiquitin conjugating enzyme (E2). J Biol Chem 267: 15116–15121 (1992).

    PubMed  Google Scholar 

  12. Courtney SE, Rider CC, Stead AD: Changes in protein ubi quitination and the expression of ubiquitin-encoding transcripts in daylily petals during floral development and senescence. Physiol Plant 91: 196–204 (1994).

    Article  Google Scholar 

  13. Demura T, Fukuda H: Novel vascular cell-specific genes whose expression is regulated temporally and spatially during vascular system development. Plant Cell 6: 967–981 (1994).

    Article  PubMed  Google Scholar 

  14. Genschik P, Durr A, Fleck J: Differential expression of several E2-type ubiquitin carrier protein genes at different developmental stages ofArabidopsis thaliana andNicotinana sylvestris. Mol Gen Genet 244: 548–556 (1994).

    PubMed  Google Scholar 

  15. Girod P-A, Carpenter TB, van Nocker S, Sullivan ML, Vierstra RD: Homologs of the-essential ubiquitin-conjugating enzymes UBC1, 4, and 5 in yeast are encoded by a multigene family inArabidopsis thaliana. Plant J 3: 545–552 (1993).

    Article  PubMed  Google Scholar 

  16. Haas AL, Baboshina O, Williams B, Schwartz LM: Coordinated induction of the ubiquitin conjugation pathway accompanies the developmentally programmed death of insect skeletal muscle. J Biol Chem 270: 9407–9412 (1995).

    Article  PubMed  Google Scholar 

  17. Hensel LL, Grbic V, Baumgarten DA, Bleecker AB: Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues inArabidopsis. Plant Cell 5: 553–564 (1993).

    Article  PubMed  Google Scholar 

  18. Jefferson RA, Kavanagh TA, Bevan MW: GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    PubMed  Google Scholar 

  19. Jentsch S: The ubiquitin conjugating system. Annu Rev Genet 26: 177–205 (1992).

    Article  Google Scholar 

  20. Kaiser P, Seufert W, Hoefferer L, Koffer B, Sachsenmaier C, Herzog H, Jentsch S, Schweiger M, Schneider R: A human ubiquitin-conjugating enzyme homologous to yeast UBC8. J Biol Chem 269: 8797–8802 (1994).

    PubMed  Google Scholar 

  21. Koken P, Reynolds P, Bootsma D, Hoeijmakers J, Prakash S, Prakash L:Dhr6, aDrosophila homolog of the yeast DNA-repair geneRAD6. Proc Natl Acad Sci USA 88: 38322–3836 (1991).

    Google Scholar 

  22. Lauzon RJ, Patton CW, Weissman IL: A morpohological and immunohistochemical study of programmed cell death inBotryllus schlosseri (Tunicata, Ascidiacea). Cell Tissue Res 272: 115–127 (1993).

    Article  PubMed  Google Scholar 

  23. Mansfield SG, Briarty LG, Erni S: Early embryogenesis inArabidopsis thaliana. I. The mature embryo sac: Can J Bot 69: 446–460 (1991).

    Google Scholar 

  24. Martin T, Wohner R-V, Hummel S, Willmitzer L, Frommer WB: The GUS reporter system as a tool for the study of plant gene expression. In: Gallagher SR (ed) Gus Protocols: using the GUS Gene as a Reporter of Gene Expression, pp. 23–43. Academic Press, San Diego, CA (1992).

    Google Scholar 

  25. Mittler R, Lam E: In situ detection of nDNA fragmentation during the differentiation of trachery elements in higher plants. Plant Physiol 108: 489–493 (1995).

    PubMed  Google Scholar 

  26. Qin S, Nakajima B, Nomura M, Arfin SM: Cloning and characterization of aSaccharomyces cerevisiae gene encoding a new member of the ubiquitin-conjugating protein family. J Biol Chem 266: 15549–15554 (1991).

    PubMed  Google Scholar 

  27. Reynolds P, Koken MHM, Hoeijmakers JHJ, Prakash S, Prakash L: Therhp6+ gene ofSchizosaccharomyces pombe: a structural and functional homolog of theRAD6 gene from the distantly related yeastSaccharomyces cerevisiae. EMBO J 9: 1423–1430 (1990).

    PubMed  Google Scholar 

  28. Scheffner M, Nuber U, Hulbregtse JM: Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 363: 81–83 (1995).

    Article  Google Scholar 

  29. Schliephacke M, Kremp A, Schmid H-P, Kohler K, Kull U: Prosomes (proteasomes) of higher plants. Eur J Cell Biol 55: 114–121 (1991).

    PubMed  Google Scholar 

  30. Schneider R, Eckerskorn C, Lottspeich F, Schweiger M: The human ubiquitin carrier protein E2 (Mr=17,000) is homologous to the yeast DNA repair geneRAD6. EMBO J 9: 1431–1435 (1990).

    PubMed  Google Scholar 

  31. Schwartz LM, Myer A, Kosz L, Engelstein M, Maier C: Activation of polyubiquitin gene expression during developmentally regulated programmed cell death. Neuron 5: 411–419 (1990).

    Article  PubMed  Google Scholar 

  32. Shimogawara K, Muto S: Purification ofChlamydomonas 28-kDa ubiquitinated protein and its identification as ubiquitinated histone H2B. Arch Biochem Biophys 294: 193–199 (1992).

    PubMed  Google Scholar 

  33. Sullivan ML, Vierstra RD: Cloning of a 16-kDa ubiquitin carrier protein (E2) from wheat andArabidopsis thaliana: Identification of functional domains byin vitro mutagenesis. J Biol Chem 266: 23878–23885 (1991).

    PubMed  Google Scholar 

  34. Sullivan ML, Callis J, Vierstra RD: HPLC resolution of ubiquitin pathway from wheat germ. Plant Physiol 94: 710–716 (1990).

    Google Scholar 

  35. Sullivan ML, Carpenter T, Vierstra RD: Homologues of wheat ubiquitin-conjugating enzymesTaUBC1 andTaUBC4 are encoded by small multigene families inArabidopsis thaliana. Plant Mol Biol 24: 651–661 (1994).

    Article  PubMed  Google Scholar 

  36. Thoma S, Hecht U, Kippers A, Botella J, de Vries S, Somerville C: Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein fromArabidopsis. Plant Physiol 105: 35–45 (1994).

    Article  PubMed  Google Scholar 

  37. Uknes S, Dincher S, Friedrich L, Negrotto D, Williams S, Thompson-Taylor H, Potter S, Ward E, Ryals J: Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell 5: 159–169 (1993).

    Article  PubMed  Google Scholar 

  38. Valvekens D, Van Montagu M, van Lusebettens M:Agrobacterium tumfaciens-mediated transformation ofArabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85: 5536–5540.

  39. Varshavsky A: The N-end rule. Cell 69: 725–735 (1992).

    Google Scholar 

  40. Vierstra RD: Protein degradation in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 385–410 (1993).

    Article  Google Scholar 

  41. Watts FZ, Butt N, Layfield P, Machuka J, Burke JF, Moore AL: Floral expression of a gene encoding an E2-related ubiquitin-conjugating protein fromArabidopsis thaliana. Plant Mol Biol 26: 445–451 (1994).

    PubMed  Google Scholar 

  42. Wing SS, Dumas F, Banville D: A rabbit reticulocyte ubiquitin carrier protein that supports ubiquitin-dependent proteolysis (E214k ) is homologous to the yeast DNA repair geneRAD6. J Biol Chem 267: 6495–6501 (1992).

    PubMed  Google Scholar 

  43. Zhen M, Heinlein R, Jones D, Jentsch S, Candido EPM: Theubc-2 gene ofCaenorhabditis elegans encodes a ubiquitin-conjugating enzyme involved in selective protein degradation. Mol Cell Biol 13: 1371–1377 (1993).

    PubMed  Google Scholar 

  44. van Nocken S, Walker JM, Vierstra RD: TheArabidopsis thaliana UBC 7/13/14 genes encode a family of multiubiquitin E2 enzymes. J Biol Chem 271: 12150–12158 (1996).

    Article  PubMed  Google Scholar 

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Thoma, S., Sullivan, M.L. & Vierstra, R.D. Members of two gene families encoding ubiquitin-conjugating enzymes, AtUBC1-3 and AtUBC4-6, fromArabidopsis thaliana are differentially expressed. Plant Mol Biol 31, 493–505 (1996). https://doi.org/10.1007/BF00042223

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  • DOI: https://doi.org/10.1007/BF00042223

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