1887

Abstract

when growing under the conventional synchronizing conditions of batch culture and intermittent illumination shows periodic changes in the rate of SO uptake and in the specific rate of S incorporation into protein relative to total protein. There are also periodic changes in the rates of synthesis of individual proteins including several chloroplast membrane proteins and of tubulin, which is synthesized maximally prior to the initiation of division events and is not synthesized during cytokinesis. Activities of citrate synthase and aspartate transcarbamoylase enzymes increase discontinuously under synchronizing conditions. These periodic events are not part of a developmental programme which is essential for division, since the periodicity disappears under constant environmental conditions. Synchronously dividing cells then show smoothly increasing rates of SO uptake into cells and of incorporation into protein. There is a constant specific rate of isotope incorporation, relative to total protein, which correlates with the exponential accumulation of protein through the cell cycle. The 300 most abundantly labelled proteins are synthesized continuously through the cell cycle and this accords with the continuous accumulation of citrate synthase and aspartate transcarbamoylase enzyme activities. Tubulin synthesis is continuous under constant growth conditions and therefore periodic increases in tubulin concentration are not an essential part of mitotic spindle or phycoplast formation. Of the sedimentable proteins only one of the 200 most abundantly labelled shows a cessation of synthesis. A previously reported periodic synthesis of chloroplast membrane proteins is not essential for chloroplast assembly in dividing cells. The significance of these data is discussed in relation to cell cycle control and it is proposed that three categories of periodic event should be recognized. Periodic syntheses of proteins that are directly involved in division processes may be classed as primary cell cycle events if they accompany the cell cycle under all growth conditions, and these events may include division-initiating processes. If periodic synthesis of such proteins occurs only under some growth conditions then their synthesis is classed as a secondary cell cycle event. Discontinuous synthesis of proteins that do not contribute directly to division processes and are only synthesized discontinuously during or in recovery from changing environmental conditions, is considered a tertiary cell cycle event, but by adapting cell structure and metabolism to environmental conditions such events may indirectly sustain division processes. It is suggested that the periodic synthesis of tubulin under synchronizing conditions is consistent with the operation of a secondary cell cycle control, but that the periodic increases in the activity of a respiratory and biosynthetic enzyme and the periodic synthesis of numerous individual unidentified proteins, under changing conditions in synchronous culture are only tertiarily related to the cell cycle.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-129-6-1899
1983-06-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/129/6/mic-129-6-1899.html?itemId=/content/journal/micro/10.1099/00221287-129-6-1899&mimeType=html&fmt=ahah

References

  1. Baum P., Thorner J., Honig L. 1978; Identification of tubulin from the yeast Saccharomyces cere- visiae. Proceedings of the National Academy of Sciences of the United States of America 75:4962–4966
    [Google Scholar]
  2. Beck D. P., Levine R. P. 1974; Synthesis of chloroplast membrane polypeptides during synchronous growth of Chlamydomonas reinhardtii. Journal of Cell Biology 63:759–772
    [Google Scholar]
  3. Best D., Warr P. J., Gull K. 1981; Influence of the composition of commercial sodium dodecyl sulfate preparations on the separation of a and p- tubulin during polyacrylamide gel electrophoresis. Analytical Biochemistry 114:281–284
    [Google Scholar]
  4. Bourguignon L. Y. W., Palade G. E. 1976; Incorporation of polypeptides into thylakoid membranes of Chlamydomonas reinhardtii. Cyclic variations. Journal of Cell Biology 69:327–344
    [Google Scholar]
  5. Brunke K. J., Collis P. S., Weeks D. P. 1982; Post-translational modification of tubulin dependent on organelle assembly. Nature, London 297:516–518
    [Google Scholar]
  6. Cooper T. G., Beevers H. 1969; Mitochondria and glyoxysomes from castor bean endosperm, enzyme constituents and catalytic capacity. Journal of Biological Chemistry 244:3507–3513
    [Google Scholar]
  7. Donachie W. D. 1981; The cell cycle of Escherichia coli. In The Cell Cycle Society for Experimental Biology, Seminar Series 10 pp 63–83 Edited by John P. C. L. Cambridge: Cambridge University Press;
    [Google Scholar]
  8. Donachie W. D., Masters M. 1969; Temporal control of gene expression in bacteria. In The Cell Cycle: Gene-Enzyme Interactions pp. 37–76 Edited by Padilla G. M., Whitson G. L., Cameron I. L. London: Academic Press;
    [Google Scholar]
  9. Donnan L., John P. C. L. 1983; Timer and sizer controls in the cell cycles of Chlamydomonas and Chlorella. In The Microbial Cell Cycle Edited by Nurse P., Streiblova E. Boca Raton: CRC Press; in the Press
    [Google Scholar]
  10. Elliott S. G., Mclaughlin C. S. 1978; Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 75:4384–4388
    [Google Scholar]
  11. Fantes P. A., Nurse P. 1981; Division timing: controls, models and mechanisms. In The Cell Cycle Society for Experimental Biology Seminar Series 10 pp. 11–33 Edited by John P. C. L. Cambridge: Cambridge University Press;
    [Google Scholar]
  12. Forde B. G., Gunning B. E. S., John P. C. L. 1976; Synthesis of the inner mitochondrial membrane and the intercalation of respiratory enzymes during the cell cycle of Chlorella. Journal of Cell Science 21:329–340
    [Google Scholar]
  13. Gerhart J. C., Pardee A. B. 1962; The enzymology of control by feedback inhibition. Journal of Biological Chemistry 237:891–896
    [Google Scholar]
  14. Gunning B. E. S., Steer M. W., Cochrane M. P. 1968; Occurrence, molecular structure and induced formation of the ‘stroma centre’ in plastids. Journal of Cell Science 3:445–456
    [Google Scholar]
  15. Halvorson H. O., Carter B. L. A., Tauro P. 1971; Synthesis of enzymes during the cell cycle. Advances in Microbial Physiology 6:47–106
    [Google Scholar]
  16. Hames B. D., Weeks G., Ashworth J. M. 1972; Glycogen synthetase and the control of glycogen synthesis in the cellular slime mould Dictyostelium discoideum during cell differentiation. Biochemical Journal 126:627–633
    [Google Scholar]
  17. Hansen J. N., Spiegelman G., Halvorson H. O. 1970; Bacterial spore outgrowth: its regulation. Science 168:1291–1298
    [Google Scholar]
  18. Hartwell L. H., Mortimer R. K., Culotti J., Culotti M. 1973; Genetic control of the cell division cycle in yeast. V. Genetic analysis of cdc mutants. Genetics 74:267–286
    [Google Scholar]
  19. Haselkorn R., Fernández-Morán H., Kieras F. J., Van Bruggen E. F. J. 1965; Electron microscopic and biochemical characterisation of fraction 1 protein. Science 150:1598–1601
    [Google Scholar]
  20. Herbert D., Elsworth R., Telling R. C. 1956; The continuous culture of bacteria; a theoretical and experimental study. Journal of General Microbiology 14:601–622
    [Google Scholar]
  21. Hiller R. G., Goodchild D. J. 1981; Thylakoid membrane and pigment organisation. In Photosynthesis, vol. 8 in The Biochemistry of Plants A Comprehensive Treatise pp. 1–49 Edited by Hatch M. D., Boardman N. K. New York: Academic Press;
    [Google Scholar]
  22. Hopkins H. A., Flora J. B., Schmidt R. R. 1972; Periodic DNA accumulation during the cell cycle of a thermophilic strain of Chlorella pyrenoidosa. Archives of Biochemistry and Biophysics 153:845–849
    [Google Scholar]
  23. Howell S. H., Naliboff J. A. 1973; Conditional mutants in Chlamydomonas reinhardtii blocked in the vegetative cell cycle. Journal of Cell Biology 57:760–772
    [Google Scholar]
  24. Howell S. H., Posakony J. W., Hill K. R. 1977; The cell cycle program of polypeptide labelling in Chlamydomonas reinhardtii. Journal of Cell Biology 72:223–241
    [Google Scholar]
  25. Janero D. R., Barrnett R. 1982; Thylakoid membrane biogenesis in Chlamydomonas reinhardi 137+. II. Cell cycle variations in the synthesis and assembly of pigment. Journal of Cell Biology 93:411–416
    [Google Scholar]
  26. John P. C. L., Mccullough W., Atkinson A.W.JR, Gunning B. E. S. 1973; The cell cycle in Chlorella. In The Cell Cycle in Development and Differentiation pp. 61–76 Edited by Balls M., Billett F. S. Cambridge: Cambridge University Press;
    [Google Scholar]
  27. John P. C. L., Lambe C. A., Mcgookin R., Orr B. 1981; Accumulation of protein and messenger RNA molecules in the cell cycle. In The Cell Cycle Society for Experimental Biology Seminar Series 10 pp. 185–221 Edited by John P. C. L. Cambridge: Cambridge University Press;
    [Google Scholar]
  28. John P. C. L., Lambe C. A., Mcgookin R., Orr B., Rollins M. J. 1982; Poly(A)+ RNA populations, polypeptide synthesis and macromolecule accumulation in the cell cycle of the eukaryote Chlorella. Journal of Cell Science 55:51–67
    [Google Scholar]
  29. Johnson U. G., Porter K. R. 1968; Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules. Journal of Cell Biology 38:403–425
    [Google Scholar]
  30. Kates J. R., Jones R. F. 1967; Periodic increases in enzyme activity in synchronised cultures of Chlamydomonas reinhardtii. Biochimica et biophysica acta 145:153–158
    [Google Scholar]
  31. Kuhl A., Lorenzen H. 1964; Handling and culturing of Chlorella. Methods in Cell Physiology 1:159–187
    [Google Scholar]
  32. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227:680–685
    [Google Scholar]
  33. Laskey R. A., Mills A. D. 1975; Quantitative film detection of 3H and 14C in polyacrylamide gels by fiuorography. European Journal of Biochemistry 56:335–341
    [Google Scholar]
  34. Lefebvre P. A., Silflow C. D., Wieben E. D., Rosenbaum J. L. 1980; Increased levels of mRNA’s for tubulin and other flagellar proteins after amputation or shortening of Chlamydomonas flagella. Cell 20:469–477
    [Google Scholar]
  35. Lien T., Knutsen G. 1976; Synchronized cultures of a wall-less mutant of Chlamydomonas reinhardii. Archives of Microbiology 108:189–194
    [Google Scholar]
  36. Linn T., Losick R. 1976; The program of protein synthesis during sporulation in Bacillus subtilis. Cell 8:103–114
    [Google Scholar]
  37. Lorenzen H., Hesse M. 1974; Synchronous cultures. In Algal Physiology and Biochemistry pp. 894–908 Edited by Stewart W. D. P. Oxford: Blackwell Scientific Publications;
    [Google Scholar]
  38. Luck D. J. L., Huang B., Piperno G. 1982; Genetics and biochemical analysis of the eukaryotic flagellum. Symposia of the Society for Experimental Biology 35:399–419
    [Google Scholar]
  39. Lutkenhaus J. F., Moore B. A., Masters M., Donachie W. D. 1979; Individual proteins are synthesized continuously throughout the Escherichia coli cell cycle. Journal of Bacteriology 138:352–360
    [Google Scholar]
  40. Minami S. A., Collis P. S., Young E. E., Weeks D. P. 1981; Tubulin induction in C. reinhardii: requirement for tubulin mRNA synthesis. Cell 24:89–95
    [Google Scholar]
  41. Mitchelson K., Chambers T., Bradbury E. M., Matthews H. R. 1978; Activation of histone kinase in G2 phase of the cell cycle in Physarum polycephalum. FEBS Letters 92:339–342
    [Google Scholar]
  42. Mitchison J. M. 1969; Enzyme synthesis in synchronous cultures. Science 165:657–663
    [Google Scholar]
  43. Mitchison J. M. 1971 The Biology of the Cell Cycle Cambridge: Cambridge University Press;
    [Google Scholar]
  44. Mitchison J. M. 1977; Enzyme synthesis during the cell cycle. In Cell Differentiation in Microorganisms Plants and Animals pp. 377–401 Edited by Nover L., Mothes K. Jena: VEB Gustav Fischer Verlag;
    [Google Scholar]
  45. Myers J., Clark L. B. 1944; Culture conditions and the development of the photosynthetic mechanism II. An apparatus for the continuous culture of Chlorella. Journal of General Physiology 28:103–112
    [Google Scholar]
  46. O’farrell P. H. 1975; High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250:4007–4021
    [Google Scholar]
  47. Pickett-Heaps J. D. 1972; Variation in mitosis and cytokinesis in plant cells: its significance in the phylogeny and evolution of ultrastructural systems. Cytobios 5:59–77
    [Google Scholar]
  48. Piperno G., Luck D. J. L. 1977; Microtubular proteins of Chlamydomonas reinhardtii. An immunochemical study based on the use of an antibody specific for the β-tubulin subunit. Journal of Biological Chemistry 252:383–391
    [Google Scholar]
  49. Ponstingl H., Krauhs E., Little M., Kempf T. 1981; Complete amino acid sequence of a tubulin from porcine brain. Proceedings of the National Academy of Sciences of the United States of America 78:2757–2761
    [Google Scholar]
  50. Pringle J. R. 1981; The genetic approach to the study of the cell cycle. In Mitosis/Cytokinesis pp. 328 Edited by Zimmerman A. M., Forer A. New York: Academic Press;
    [Google Scholar]
  51. Schmidt R. R. 1974; Transcriptional and post-transcriptional control of enzyme levels in eucaryotic microorganisms. In Cell Cycle Controls pp. 201–233 Edited by Padilla G. M., Cameron I. L., Zimmerman A. H. London: Academic Press;
    [Google Scholar]
  52. Schötz F., Bathelt H., Arnold C.-G., Schimmer O. 1972; Die Architektur und Organisation der Chlamydomonas-zeWe. Ergebnisse der Elektronen-mikroskopie von Serienschnitten und der daraus resultierenden dreidimensionalen Rekonstruktion. Protoplasma 75:229–254
    [Google Scholar]
  53. Silflow C. D., Rosenbaum J. L. 1981; Multiple a- and β-tubulin genes in Chlamydomonas and regulation of tubulin mRNA levels after deflagellation. Cell 24:81–88
    [Google Scholar]
  54. Sueoka N., Chiang K.-S., Kates J. R. 1967; Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi. Journal of Molecular Biology 25:47–66
    [Google Scholar]
  55. Sussman M., Brackenbury R. 1976; Biochemical and molecular-genetic aspects of cellular slime mold development. Annual Review of Plant Physiology 27:229–265
    [Google Scholar]
  56. Tuchman J., Alton T., Lodish H. F. 1974; Preferential synthesis of actin during early development of the slime mold Dictyostelium discoideum. Developmental Biology 40:116–128
    [Google Scholar]
  57. Valenzuela P., Quiroga M., Zaldivar J., Rutter W. J., Kirschner M. W., Cleveland D. W. 1981; Nucleotide and corresponding amino acid sequences encoded by α and β tubulin mRNA’s. Nature, London 289:650–655
    [Google Scholar]
  58. Weeks D. P., Collis P. S. 1979; Induction and synthesis of tubulin during the cell cycle and life cycle of Chlamydomonas reinhardi. Developmental Biology 69:400–407
    [Google Scholar]
  59. Weingarten M. D., Suter M. M., Littman D. R., Kirschner M. W. 1974; Properties of the depolymerisation products of microtubules from mammalian brain. Biochemistry 13:5529–5537
    [Google Scholar]
  60. Witman G. B., Carlson K., Berliner J., Rosenbaum J. L. 1972; Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes and mastigonemes. Journal of Cell Biology 54:507–539
    [Google Scholar]
  61. Wollman F-A., Olive J., Bennoun P., Recouvreur M. 1980; Organisation of the photosystem II centers and their associated antennae in the thyla- koid membranes: a comparative ultrastructural, biochemical and biophysical study of Chlamydomonas wild type and mutants lacking in photosystem II reaction centers. Journal of Cell Biology 87:728–735
    [Google Scholar]
  62. Wolosker H. B. M., Dealmeida D. F. 1979; Quantitative assessment of the synchronization of cell populations. Journal of General Microbiology 110:225–227
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-129-6-1899
Loading
/content/journal/micro/10.1099/00221287-129-6-1899
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error