Skip to main content
SpringerLink
Log in

The relatively large beta-tubulin gene family of Arabidopsis contains a member with an unusual transcribed 5′ noncoding sequence

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have characterized the beta-tubulin gene family of Arabidopsis thaliana. Five distinct genes were cloned and analyzed by restriction enzyme mapping and cross-hybridization studies. Three of the genes appear to be dispersed, whereas two others are linked within 1.5 kb of one another. The two linked genes are closely related and appear to have resulted from a fairly recent duplication. The three dispersed genes do not cross-hybridize to one another or to the two linked genes under highly stringent hybridization conditions, suggesting that they arose from more ancient duplications. From Southern analysis we estimate that there are a total of between six and ten beta-tubulin genes in Arabidopsis. Additional analyses indicate that the gene family is equal in size or larger than those in other plants, but significantly smaller than those in related Brassica species. Sequence determination of one of the Arabidopsis genes revealed a highly unusual transcribed leader sequence. The leader contains two fairly long tracks of adenines. One is located toward the 5′ end of the mRNA and the other is just before the initiation codon. A track of uridines is located between the adenine tracks. This leader can form two different secondary structures that may have regulatory significance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bennett MD, Smith JB: Nuclear DNA amounts in angiosperms. Phil Transactions Royal Soc London 274: 227–274 (1976).

    Google Scholar 

  2. Benoist C, O'Hare K, Breathnach R, Chambon P: The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res 8: 127–142 (1980).

    Google Scholar 

  3. Benton WD, Davis RW: Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196: 180–182 (1977).

    Google Scholar 

  4. Berk AJ, Sharp PA: Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease digested hybrids. Cell 12: 721–732 (1977).

    Google Scholar 

  5. Brown JWS: A catalogue of splice junction and putative branch point sequences from plant introns. Nucleic Acids Res 14: 9549–9559 (1986).

    Google Scholar 

  6. Brunke KJ, Anthony JG, Sternberg EJ, Weeks DP: Repeated consensus sequence and pseudopromoters in the four coordinately regulated tubulin genes of Chlamydomonas reinhardi. Mol Cell Biol 4: 1115–1124 (1984).

    Google Scholar 

  7. Brunke KJ, Young EE, Buchbinder BU, Weeks DP: Coordinate regulation of the four tubulin genes of Chlamydomonas reinhardi. Nucleic Acids Res 10: 1295–1310 (1982).

    Google Scholar 

  8. Caron JM, Kirschner MW: Autoregulation of tubulin synthesis. Bio Essays 5: 211–216 (1987).

    Google Scholar 

  9. Cerff R, Hundrieser J, Friedrich R: Subunit B of chloroplast glyceraldehyde-3-phosphate dehydrogenase is related to β-tubulin. Mol Gen Genet 204: 44–51 (1986).

    Google Scholar 

  10. Chang C, Meyerowitz EM: Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci 83: 1408–1412 (1986).

    Google Scholar 

  11. Dale RMK, McClure BA, Houchins JP: A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: Application to sequencing the corn mitochondrial 18 S rDNA. Plasmid 13: 31–40 (1985).

    Google Scholar 

  12. Dawson PJ, Lloyd CW: Identification of multiple tubulins in taxol microtubules purified from carrot suspension cells. EMBO J 4: 2451–2455 (1985).

    Google Scholar 

  13. Dustin P: Microtubules. Springer-Verlag, Berlin (1984).

    Google Scholar 

  14. Feldmann KA, Marks MD: Rapid and efficient regeneration of plants from explants of Arabidopsis thaliana. Plant Science 47: 63–69 (1986).

    Google Scholar 

  15. Feldmann KA, Marks MD: Agrobacterium-mediated transformation of germinating seeds of Arabidopsis thaliana: A non-tissue culture approach. Mol Gen Biol 108: 1–9 (1987).

    Google Scholar 

  16. Gunning BES, Hardham AR: Microtubules. Annu Rev Plant Physiol 33: 651–698 (1982).

    Google Scholar 

  17. Karlin-Neumann GA, Tobin EM: Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 9–13 (1986).

    Google Scholar 

  18. Kimmel BE, Samson S, Wu J, Hirschberg R, Yarbrough R: Tubulin genes of the African trypanosome Trypanosoma brucei rhodesiense: nucleotide sequence of a 3.7-kb fragment containing genes for alpha and beta tubulins. Gene 35: 237–248 (1985).

    Google Scholar 

  19. Kozak M: Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci USA 83: 2850–2854 (1986).

    Google Scholar 

  20. Krauhs E, Little M, Kempf T, Hofer-Warbinek R, Wolfgang A, Ponstingl H: Complete amino acid sequence of β-tubulin from porcine brain. Proc Natl Acad Sci 78: 4156–4160 (1981).

    Google Scholar 

  21. Lerner MR, Boyle JA, Mount SM, Wolin SL, Are snRNPs involved in splicing. Nature 283: 220–224 (1980).

    Google Scholar 

  22. Leutwiler LS, Meyerowitz EM, Tobin EM: Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res 14: 4051–4064 (1986).

    Google Scholar 

  23. Lloyd AM, Barnason AR, Rogers SG, Byrne MC, Fraley RT, Horsch RB: Transformation of Arabidopsis thaliana with Agrobacterium tumefaciens. Science 234: 464–466 (1986).

    Google Scholar 

  24. Luduena RF, Woodward DO: Isolation and partial characterization of α- and β-tubulin from outer doublets of seaurchin sperm and microtubules of chick-embryo brain. Proc Natl Acad Sci USA 70: 3594–3598 (1973).

    Google Scholar 

  25. Maniatis T, Fritsch E, Sambrook J: In: Molecular Cloning. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  26. Marks MD, Lindell JS, Larkins BA: Nucleotide sequence analysis of zein mRNAs from maize endosperm. J Biol Chem 260: 16451–16459 (1985).

    Google Scholar 

  27. May GS, Tsang ML, Smith H, Fidel S, Morris NR: Beta-tubulin genes of Aspergillus nidulans are unusually divergent. Gene, in press (1987).

  28. Meyerowitz EM, Pruitt RE: Arabidopsis thaliana and plant molecular genetics. Science 229: 1214–1218 (1985).

    Google Scholar 

  29. Morejohn LC, Fosket DE: Tubulins from plants, fungi, and protists. A review. In: Shay J (ed.) Cellular and Molecular Biology of the Cytoskeleton. Plenum, New York (1986).

    Google Scholar 

  30. Neff NF, Thomas JH, Grisafi P, Botstein D: Isolation of the β-tubulin gene from yeast and demonstration of its essential function in vivo. Cell 33: 211–219 (1983).

    Google Scholar 

  31. Norrander J, Kempe T, Messing J: Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26: 101–106 (1983).

    Google Scholar 

  32. Orbach MJ, Porro EB, Yanofsky C: Cloning and characterization of the gene for β-tubulin from a benomyl-resistant mutant of Neurospora crassa and its use as a dominant selectable marker. Mol Cell Biol 6: 2452–2461 (1986).

    Google Scholar 

  33. Pelletier J, Sonenberg N: Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 40: 515–526 (1985).

    Google Scholar 

  34. Proudfoot NJ: Eukaryotic promoters? Nature 279: 376 (1979).

    Google Scholar 

  35. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  36. Sheikholeslam SN, Weeks DP: Acetosyringone promotes high efficiency transformation of Arabidopsis thaliana by Agrobacterium tumefaciens. Plant Mol Biol 8: 291–298 (1987).

    Google Scholar 

  37. Shih M-C, Lazar G, Goodman H: Evidence in favor of the symbiotic origin of chloroplasts: Primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases. Cell 47: 73–80 (1986).

    Google Scholar 

  38. Somerville CR, McCourt P, Caspar T, Estelle M, Keith K: Arabidopsis thaliana as a model system for plant genetics and molecular biology. In: Freeling M (ed.) Plant Genetics. Alan R. Liss, New York (1985) pp 651–660.

    Google Scholar 

  39. Southern E: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517 (1975).

    Google Scholar 

  40. Sullivan KF, Lau JTY, Cleveland DW: Apparent gene conversion between β-tubulin genes yields multiple regulatory pathways for a single β-tubulin polypeptide isotype. Mol Cell Biol 5: 2454–2465 (1985).

    Google Scholar 

  41. Sures I, Crippa M: Xenopsin: The neurotensin-like octapeptide from Xenopus skin at the carbosyl terminus of its precursor. Proc Natl Acad Sci USA 81: 380–384 (1984).

    Google Scholar 

  42. Weeks DP, Beerman N, Griffith OM: A small-scale five-hour procedure for isolating multiple samples of CsCl-purified DNA: Application to isolations from mammalian, insect, higher plant, algal, yeast, and bacterial sources. Anal Biochem 152: 376–385 (1986).

    Google Scholar 

  43. Yamamoto KR, Alberts BM: Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large scale virus purification. Virology 40: 734–744 (1970).

    Google Scholar 

  44. Youngblom J, Schloss JA, Silflow CD: The two β-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Mol Cell Biol 4: 2686–2696 (1984).

    Google Scholar 

Download references

Author information

Author notes

  1. M. David Marks

    Present address: School of Biological Sciences, University of Nebraska, 68588-0118, Lincoln, NE, USA

Authors and Affiliations

  1. Sandoz Crop Protection Corp., Zoecon Research Institute, 975 California Ave., 94304, Palo Alto, CA, USA

    M. David Marks, Joanne West & Donald P. Weeks

Authors
  1. M. David Marks
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanne West
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donald P. Weeks
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marks, M.D., West, J. & Weeks, D.P. The relatively large beta-tubulin gene family of Arabidopsis contains a member with an unusual transcribed 5′ noncoding sequence. Plant Mol Biol 10, 91–104 (1987). https://doi.org/10.1007/BF00016147

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00016147

Key words

Search

Navigation