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Volume 138, Issue 1

Preferential expression of one β-tubulin gene during flagellate development in Free

Abstract

Summary: The microbial eukaryote displays several distinct cell types in its life cycle, including amoebae, flagellates and plasmodia. Despite its relative simplicity, has a tubulin gene family of complexity comparable to that of . We have identified β-tubulin cDNAs from that are derived from the β-tubulin locus and encode β1A tubulin. We have also identified a partial cDNA for the unlinked β-tubulin gene, which encodes β1B tubulin. The polypeptide sequences encoded by and show 99% identity, but the nucleotide sequences show only 85% identity, consistent with an ancient duplication of these genes. The gene is expressed in amoebae, flagellates and plasmodia, whereas is expressed only in amoebae and flagellates. During the amoeba-flagellate transition the level of transcript increases over 100-fold, while the level of transcript changes very little. Thus has a mechanism for regulating the level of discrete β-tubulin transcripts differentially during flagellate development. A need for this differential regulation could account for the maintenance of the virtually isocoding and β-tubulin genes.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Society for General Microbiology 1992
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1992-01-01
2024-04-26
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References

  1. AVIV H., LEDER P. 1972; Purification of biologically active globin messenger RNA by chromatography on oligothymidyiic acid cellulose. Proceedings of the National Academy of Sciences of the United States of America 69:1408–1418
     [Google Scholar]
  2. BAKER E. J., SCHLOSS J. A., ROSENBAUM J. L. 1984; Rapid changes in tubulin RNA synthesis and stability induced by deflagellation in Chlamydomonas . Journal of Cell Biology 99:2074–2081
     [Google Scholar]
  3. BIRKETT C. R., FOSTER K. E., JOHNSON L., GULL K. 1985; Use of monoclonal antibodies to analyse the expression of a multitubulin gene family. FEBS Letters 187:211–218
     [Google Scholar]
  4. BRUNKE K. J., YOUNG E. E., BUCHBINDER B. U., WEEKS D. P. 1982; Coordinate regulation of the four tubulin genes of Chlamydomonas reinhardi . Nucleic Acids Research 10:1295–1310
     [Google Scholar]
  5. BURLAND T. G., GULL K., SCHEDL T., BOSTON R. S., DOVE W. F. 1983; Cell-type dependent expression of tubulins in Physarum . Journal of Cell Biology 97:1852–1859
     [Google Scholar]
  6. BURLAND T. G., SCHEDL T., GULL K., DOVE W. F. 1984; Genetic analysis of resistance to benzimidazoles in Physarum : differential expression of beta tubulin genes. Genetics 108:123–141
     [Google Scholar]
  7. BURLAND T. G., PAUL E. C. A., OETLIKER M., DOVE W. F. 1988; A gene encoding the major beta-tubulin of the mitotic spindle in Physarum polycephalum plasmodia. Molecular and Cellular Biology 8:1275–1281
     [Google Scholar]
  8. COOKE D. J., DEE J. 1975; Methods for the isolation and analysis of plasmodial mutants in Physarum polycephalum . Genetical Research 24:175–187
     [Google Scholar]
  9. DALE R. M. K., MCCLURE B. A., HOUCHINS J. P. 1985; A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the com mitochondrial 18S rDNA. Plasmid 13:31–40
     [Google Scholar]
  10. DEE J., FOXON J. L., ANDERSON R. W. 1989; Growth, development and genetic characteristics of Physarum polycephalum amoebae able to grow in liquid, axenic medium. Journal of General Microbiology 135:1567–1588
     [Google Scholar]
  11. DIGGINS-GILICINSKI M., SOLNICA-KREZEL L., BURLAND T. G., PAUL E. C. A., DOVE W. F. 1989; The localization of the divergent β2-tubulin in the microtubular arrays of Physarum polycephalum . Journal of Cell Science 94:217–226
     [Google Scholar]
  12. FULTON C., SIMPSON P. A. 1976 Selective synthesis and utilization of flagellar tubulin: the multi-tubulin hypothesis. In Cell Motility pp 987–1005 Edited by Goldman R., Pollard T., Rosenbaum J. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  13. GONG Z., BRANDHORST B. P. 1987; Stimulation of tubulin gene transcription by deciliation of sea urchin embryos. Molecular and Cellular Biology 7:4238–4246
     [Google Scholar]
  14. GREEN L., DOVE W. F. 1984; Tubulin proteins and RNA during the myxamoeba-flagellate transformation of Physarum polycephalum . Molecular and Cellular Biology 4:1706–1711
     [Google Scholar]
  15. HARLOW P., NEMER M. 1987; Developmental and tissue-specific regulation of β-tubulin gene expression in the embryo of the sea urchin Strongylocentrotus purpuratus . Genes and Development 1:147–160
     [Google Scholar]
  16. HOYLE H. D., RAFF E. C. 1990; Two Drosophila bet’ tubulin isoforms are not functionally equivalent. Journal of Cell Liology 111:1009–1026
     [Google Scholar]
  17. HUYNH T. V., YOUNG R. A., DAVIS R. W. 1984 Constructing and screening cDNA libraries in lambda gtlO and lambda gtl1. In DNA Cloning Techniques: A Practical Approach pp 49–78 Edited by Glover D. Oxford: IRL Press;
     [Google Scholar]
  18. JOSHI H. C, CLEVELAND D. W. 1989; Differential utilization of fl- tubulin isotypes in differentiating neurites. Journal of Cell Biology 109:663–675
     [Google Scholar]
  19. KILMARTIN J. V., WRIGHT B., MILSTEIN C. 1982; Rat monoclonal antitubulin antibodies derived using a new non-secreting rat cell line. Journal of Cell Biology 93:576–582
     [Google Scholar]
  20. LAI E.Y, REMILLARD S. P., FULTON C. 1988; The α-tubulin gene family expressed during cell differentiation in Naegleria gruberi . Journal of Cell Biology 106:2035–2046
     [Google Scholar]
  21. LASKEY R. A., MILLS A. D. 1977; Enhanced autoradiographic detection of 32P and 125I using intensifying screens and hypersensitized films. FEBS Letters 82:314–322
     [Google Scholar]
  22. LEE J. H., WALSH C. J. 1988; Transcriptional regulation of coordinate changes in flagellar mRNAs during differentiation of Naegleria gruberi amebae into flagellates. Molecular and Cellular Biology 8:2280–2287
     [Google Scholar]
  23. LEFEBVRE P. A., ROSENBAUM J. L. 1986; Regulation of the synthesis and assembly of ciliary and flagellar proteins during regeneration. Annual Review of Cell Biology 2:517–546
     [Google Scholar]
  24. LEWIS S. A., Gu W., COWAN N. J. 1987; Free intermingling of mammalian β-tubulin isotypes among functionally distinct microtubules. Cell 49:539–548
     [Google Scholar]
  25. MELTON D. A., KREIG P. A., REBAGLIATI M. R., MANIATIS T., ZINN K., GREEN M. R. 1984; Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Research 12:7035–7070
     [Google Scholar]
  26. MERCER J. F. B., WAKE S. A. 1985; An analysis of the rate of metallothionein mRNA poly(A) shortening using RNA blot hybridization. Nucleic Acids Research 13:7929–7943
     [Google Scholar]
  27. NEEDLEMAN S. B., WUNSCH C. D. 1970; A general method applicable to the search for similarities in the amino acid sequence of two proteins. Journal of Molecular Biology 48:443–453
     [Google Scholar]
  28. PAUL E. C. A., BURLAND T. G., GULL K. 1989; Location of a single β-tubulin gene product in both cytoskeletal and mitotic- spindle microtubules in Physarum polycephalum . Journal of General Microbiology 135:623–628
     [Google Scholar]
  29. RAFF E. C. 1984; Genetics of microtubule systems. Journal of Cell Biology 99:1–10
     [Google Scholar]
  30. RIGBY P. W., DIECKMAN M., RHODES C., BERG P. 1977; Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. Journal of Molecular Biology 113:237–332
     [Google Scholar]
  31. SANCHEZ F., NATZLE J. E., CLEVELAND D. W., KIRSCHNER M. W., MCCARTHY B. J. 1980 A dispersed multigene family encoding tubulin in Drosophila melanogaster Cell 22:845–854
     [Google Scholar]
  32. SANGER F., NICKLEN S., COULSON A. R. 1977; DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America 74:5463–5467
     [Google Scholar]
  33. SCHEDL T., BURLAND T. G., GULL K., DOVE W. F. 1984a; Cell cycle regulation of tubulin RNA level, tubulin protein synthesis, and assembly of microtubules in Physarum . Journal of Cell Biology 99:155–165
     [Google Scholar]
  34. SCHEDL T., OWENS J., DOVE W. F., BURLAND T. G. 1984b; Genetics of the tubulin gene families of Physarum . Genetics 108:143–164
     [Google Scholar]
  35. SINGHOFER-WOWRA M., CLAYTON L., DAWSON P., GULL K., LITTLE M. 1986; Amino-acid sequence data of β-tubulin from Physarum polycephalum myxamoebae. European Journal of Biochemistry 161:669–679
     [Google Scholar]
  36. SOLNICA-KREZEL L., DOVE W. F., BURLAND T. G. 1988; Activation of a β-tubulin gene during early development of the plasmodium in Physarum polycephalum . Journal of General Microbiology 134:1323–1331
     [Google Scholar]
  37. SOLNICA-KREZEL L., DIGGINS-GILICINSKI M., BURLAND T. G., DOVE W. F. 1990; Variable pathways for developmental changes in composition and organization of microtubules in Physarum polycephalum . Journal of Cell Science 96:383–393
     [Google Scholar]
  38. SOUTHERN E. M. 1975; Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98:503–517
     [Google Scholar]
  39. SULLIVAN K. F. 1988; Structure and utilization of tubulin isotypes. Annual Reviews of Cell Biology 4:687–716
     [Google Scholar]
  40. VALENZUELA P., QUIROGA M., ZALDIVAR J., RUTTER W. J., KIRSCHNER M. W., CLEVELAND D. W. 1979 Nucleotide and corresponding amino acid sequences encoded by α and β tubulin mRNAs. Nature London: 289650–655
     [Google Scholar]
  41. WALDEN E. D., BLINDT A. B., BIRKETT C. R., COX R. A., GULL K. 1989; Recognition of specific Physarum α-tubulin isotypes by a monoclonal antibody. European Journal of Biochemistry 185:383–389
     [Google Scholar]
  42. WERENSKIOLD A. K., POETSCH B., HAUGLI F. 1988; Cloning and expression of a β-tubulin gene of Physarum polycephalum . FEBS Letters 243:491–495
     [Google Scholar]
  43. YEN T. J., GAY D. A., PACHTER J. S., CLEVELAND D. W. 1988; Autoregulated changes in stability of polyribosome-bound β-tubulin mRNAs are specified by the first 13 translated nucleotides. Molecular and Cellular Biology 8:1224–1235
     [Google Scholar]
  44. YOUNGBLOOM J., SCHLOSS J. A., SILFLOW C. D. 1984; The two β-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Molecular and Cellular Biology 4:2686–2696
     [Google Scholar]
  45. ZEHNBAUER B. A., BLATTNER F. R. 1982 Construction and screening of recombinant DNA libraries with Charon vector phages. In Genetic Engineering vol 4 pp 249–279 Edited by Setlow J. K., Hollaender A. New York: Plenum;
     [Google Scholar]
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Preferential expression of one β-tubulin gene during flagellate development in Physarum
Microbiology 138, 229 (1992); https://doi.org/10.1099/00221287-138-1-229
/content/journal/micro/10.1099/00221287-138-1-229
/content/journal/micro/10.1099/00221287-138-1-229
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