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Expression of ubiquitin genes in Chlamydomonas reinhardtii: involvement in stress response and cell cycle

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Abstract

Applying different stresses (heat shock, photoinhibition, and chilling) to the unicellular green alga Chlamydomonas reinhardtii led to a characteristic transcription pattern of mRNAs encoding ubiquitin extension proteins [0.7-kb transcript(s)] as well as polyubiquitin (2.3-kb transcript). Heat shock resulted in an increase in the amount of polyubiquitin mRNA (up to tenfold compared with control cells). Chilling in the light led to a sevenfold increase in the amount of 2.3-kb transcript and to a twofold increase in the amount of 0.7-kb mRNA(s), whereas a less pronounced effect on the level of the polyubiquitin transcript was observed after applying either chilling in darkness or photoinhibition. The latter stress, however, led to a dramatic decrease in mRNAs encoding ubiquitin extension proteins (down to 23% of control cells). Experiments performed with a temperature-sensitive cell-cycle mutant of C. reinhardtii showed that the 2.3-kb polyubiquitin mRNA was no longer transcribed when cells were shifted to a non-permissive temperature, and thus were blocked in their vegetative cell cycle. This leads to the assumption that the expression of the corresponding gene is necessary for completion of the C. reinhardtii vegetative cell cycle.

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Abbreviations

bp:

base pair

kb:

kilo base

ts:

temperatures sensitive

UBI1 and 3:

ubiquitin-encoding cDNAs from C. reinhardtii

UBM:

ubiquitin-encoding part of UBI1 from C. reinhardtii

UbCEP(s):

ubiquitin extension protein(s), composed of ubiquitin followed by a C-terminal extension of either 52 or 76–81 amino acids

References

  • Adamska I, Kloppstech K, Ohad I (1993) Early light-inducible protein in pea is stable during light stress but is degraded during recovery at low light intensity. J Biol Chem 268: 5438–5444

    Google Scholar 

  • Arnasson T, Ellison MJ (1994) Stress resistance in Saccharomyces cerevisiae is strongly correlated with assembly of a novel type of multiubiquitin chain. Mol Cell Biol 14: 7876–7883

    Google Scholar 

  • Callis J, Raasch JA, Vierstra RD (1990) Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem 265: 12486–12493

    CAS  PubMed  Google Scholar 

  • Cattivelli L, Bartels D (1990) Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93: 1504–1510

    Google Scholar 

  • Chau V, Tobias JW, Bachmair A, Marriot D, Ecker DJ, Gonda DK, Vashavsky A (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243: 1576–1583

    Google Scholar 

  • Chirgwin JM, Przybyla AE, MacDonald RI, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299

    CAS  PubMed  Google Scholar 

  • Chollet R, Anderson LL (1977) Conformational changes associated with the reversible cold inactivation of ribulose-1,5-bisphosphate carboxylase-oxygenase. Biochim Biophys Acta 482: 228–240

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Deveraux Q, Ustrell V, Pickart C, Rechsteiner M (1994) A 26 protease subunit that binds ubiquitin conjugates. J Biol Chem 269: 7059–7061

    Google Scholar 

  • Finley D, Özkaynak E, Varshavsky A (1987) The yeast polyubiquitin gene is essential for resistance to high temperature, starvation, and other stresses. Cell 48: 1035–1046

    Google Scholar 

  • Finley D, Bartel B, Varshavsky A (1989) The tails of ubiquitin precursors are ribosomal proteins whose fusions to ubiquitin facilitates ribosome biogenesis. Nature 338: 394–401

    Article  CAS  PubMed  Google Scholar 

  • Gabarino JE, Rockhold DR, Belknap WR (1992) Expression of stress-responsive ubiquitin genes in potato tubers. Plant Mol Biol 20: 235–244

    Google Scholar 

  • Genschick P, Parmentier Y, Durr A, Marbach J, Criqui MC, Jamet E, Fleck J (1992) Ubiquitin genes are differentially regulated in protoplast-derived cultures of Nicotiana sylvestris and in response to various stress conditions. Plant Mol Biol 20: 879–910

    Google Scholar 

  • Gindin E, Borochov A (1992) Ubiquitin conjugation to protein increases following chilling of Clerodendrum leaves. Plant Physiol 100: 1392–1395

    Google Scholar 

  • Hoffman NE, Ko K, Milkowski D, Pichersky E (1991) Isolation and characterization of tomato cDNA and genomic clones encoding the ubiquitin gene ubi3. Plant Mol Biol 17: 1189–1202

    Google Scholar 

  • Hough R, Pratt G, Rechsteiner M (1987) Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J Biol Chem 262: 8303–8313

    Google Scholar 

  • Howell SH, Naliboff JA (1973) Conditional mutants in Chlamydomonas reinhardtii blocked in the vegetative cell cycle. I. An analysis of cell cycle block points. J Cell Biol 57: 760–772

    Google Scholar 

  • Jamet E, Durr A, Parmentier Y, Criqui MC, Fleck J (1990) Is ubiquitin involved in the dedifferentiation of higher plant cells? Cell Differ Dev 29: 37–46

    Google Scholar 

  • Krebber H, Woestmann C, Bakker-Grunwald T (1994) Evidence for the existence of a single ubiquitin gene in Giardia lamblia. FEBS Lett 343: 234–236

    Google Scholar 

  • Müller-Taubenberger A, Hagemann J, Noegel A, Gerisch G (1988) Ubiquitin gene expression in Dictyostelium is induced by heat and cold shock, cadmium, and inhibitors of protein synthesis. J Cell Sci 90: 51–5800

    Google Scholar 

  • Pollmann L, von Kampen J, Wettern M (1991) Ubiquitin in a lower plant. Characterization of ubiquitin-encoding DNA and RNA from Chlamydomonas reinhardtii. Eur J Biochem 202: 197–204

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual (2nd edn), CSHL-Press, Cold Spring Harbor

    Google Scholar 

  • Schiedlmeier B, Schmitt R (1994) Repetitious structure and transcription controls of a polyubiquitin gene in Volvox carteri. Curr Genet 25: 169–177

    Google Scholar 

  • Schulz M, Wolf D, Schnabl H (1993) Age dependent appearance of polypepties with immunoreactivity to ubiquitin antibodies in chloroplast membranes of Vicia faba L. J Plant Physiol 141: 298–303

    Google Scholar 

  • Thompson WF, White MJ (1991) Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42: 423–466

    Google Scholar 

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

    Google Scholar 

  • von Gromoff ED, Treier U, Beck CF (1989) Three light-inducible heat shock genes of Chlamydomonas reinhardtii. Mol Cell Biol 9: 3911–3918

    Google Scholar 

  • von Kampen J, Wettern M (1991) Ubiquitin-encoding mRNA and mRNA recognized by genes encoding ubiquitin-conjugating enzymes are differentially expressed in division-synchronized cultures of Chlamydomonas reinhardtii. Eur J Cell Biol 55: 312–317

    Google Scholar 

  • von Kampen J, Nieländer U, Wettern M (1994) Stress-dependent transcription of a gene encoding a Gβ-like polypeptide from Chlamydomonas reinhardtii. J Plant Physiol 143: 756–758

    Google Scholar 

  • Wettern M, von Kampen J (1992) On the molecular evolution of ubiquitin. Endocytobios Cell Res 8: 139–149

    Google Scholar 

  • Wettern M, Parag HA, Pollmann L, Ohad I, Kulka RG (1990) Ubiquitin in Chlamydomonas reinhardtii. Distribution in the cell and effect of heat shock and photoinhibition on its conjugate pattern. Eur J Biochem 191: 571–557

    Google Scholar 

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Correspondence to Michael Wettern.

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We thank Elizabeth Harris (Chlamydomonas Genetics Center, Duke University, Durham, N.C., USA) very much for making temperature-sensitive mutant strains of C. reinhardtii available to us. We are also grateful to Ildiko Kovacs and Jay Coggan (Hopkins Marine Station, Stanford University, Pacific Grove, Calif., USA) for valuable comments on the manuscript and Kathleen Greger and Kai Schledzewski (Botanisches Institut, TU Braunschweig, Germany) for the help with computer drawings.

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von Kampen, J., Nieländer, U. & Wettern, M. Expression of ubiquitin genes in Chlamydomonas reinhardtii: involvement in stress response and cell cycle. Planta 197, 528–534 (1995). https://doi.org/10.1007/BF00196675

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  • DOI: https://doi.org/10.1007/BF00196675

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