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Plant Molecular Biology

, Volume 37, Issue 6, pp 1069–1078 | Cite as

Maize α-tubulin genes are expressed according to specific patterns of cell differentiation

  • Xavier Uribe
  • Miguel Angel Torres
  • Montserrat Capellades
  • Pere Puigdomènech
  • Joan Rigau
Article

Abstract

In the past few years many α- and β-tubulin genes of different organisms have been cloned and studied, and in most systems studied they constitute multigene families. In plants, most studies have been done in Arabidopsis thaliana and Zea mays. In this paper, the study of mRNA accumulation by in situ hybridization and the activity of three maize α-tubulin gene promoters (tua1, tua2 and tua3) in transgenic tobacco plants are described. In maize, the expression of these three tubulin isotypes differ in the root and shoot apex and is associated with different groups of cells throughout the distinct stages of cell differentiation. In transgenic tobacco plants the promoters of the genes, fused to the uidA reporter gene (GUS), direct expression to the same tissues observed by in situ hybridization experiments. The tua1 promoter is mainly active in cortex-producing meristematic cells and in pollen, whereas tua3 is active in cells which are differentiating to form vascular bundles in the root and shoot apices. The accumulation of tua2 mRNA is detected by RNA blot in a similar form as tua1, but at a very much low level. In situ hybridization indicates that the tua2 mRNA specifically accumulates in the maize root epidermis. No GUS staining was detected in transgenic tobacco plants with the tua2 promoter. The difference in expression of the specific genes may be linked to processes where microtubules have different functions, suggesting that in plants, as in animals, there are differences in the function of the tubulin isotypes.

in situ hybridization maize promoter analysis tobacco transformation tubulin 

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References

  1. 1.
    Atanassova R, Chaubet N, Gigot C: A 126 bp fragment of a plant histone gene promoter confers preferential expression in meristem of transgenic Arabidopsis. Plant J 2: 291–300 (1992).Google Scholar
  2. 2.
    Baluska F, Parker JS, Barlow PW: Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J Cell Biol 103: 191–200 (1992).Google Scholar
  3. 3.
    Bonfante-Fasolo P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomènech P: Specific activation of a maize a-tubulin gene promoter in mycorrhizal transgenic tobacco plants. Plant J 9: 737–743 (1996).Google Scholar
  4. 4.
    Bonfante-Fasolo P, Perotto S: Plants and endomycorrhizal fungi: the cellular and molecular basis of their interaction. In: Verma PS (ed) Molecular Signals in Plant-Microbe Communications, pp. 445–470. CRC Press, London (1992).Google Scholar
  5. 5.
    Carpenter JL, Ploense SE, Snustad DP, Silflow CD: Preferential expression of an alpha-tubulin gene of Arabidopsis in pollen. Plant Cell 4: 557–571 (1992).CrossRefPubMedGoogle Scholar
  6. 6.
    Cleveland DW, Sullivan KF: Molecular biology and genetics of tubulin. Annu Rev Biochem 54: 331–365 (1985).CrossRefPubMedGoogle Scholar
  7. 7.
    De Pater S, Pham K, Chua NH, Memelink J, Kijne J: A 22-bp fragment of the pea lectin promoter containing essential TGAC-like motifs confers seed-specific gene expression. Plant Cell 5: 877–886 (1993).CrossRefPubMedGoogle Scholar
  8. 8.
    Dolfini S, Consonni G, Mereghetti M, Tonelli C: Antiparallel expression of the sense and antisense transcripts of maize alpha-tubulin genes. Mol Gen Genet 241: 161–169 (1993).PubMedGoogle Scholar
  9. 9.
    Fulton C, Simpson PA: Selective synthesis and utilization of flagellar tubulin. The multitubulin hypothesis. In: Goldman R, Pollard T, Rosenbaum J (eds) Cell Motility, pp. 987–1005. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1976).Google Scholar
  10. 10.
    Gamborg OL: Media preparation. In: Lindsay (ed) Plant Tissue Culture Manual, pp. 1–24. Kluwer Academic Publishers, Dordrecht, Netherlands (1991).Google Scholar
  11. 11.
    Gunning BES, Hardham AR: Microtubules. Annu Rev Plant Physiol 33: 651–698 (1982).CrossRefGoogle Scholar
  12. 12.
    Hussey PJ, Traas JA, Gull K, Lloyd CW: Isolation of cytoskeletons from synchronized plant cells: the interphase microtubule array utilizes multiple tubulin isotypes. J Cell Sci 88: 225–230 (1987).Google Scholar
  13. 13.
    Hutchens JA, Hoyle HD, Turner FR, Raff EC: Structurally similar Drosophila alpha-tubulins are functionally distinct in vivo. Mol Biol Cell 8: 481–500 (1997).PubMedGoogle Scholar
  14. 14.
    Jefferson RA: Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5: 387–405 (1987).Google Scholar
  15. 15.
    Jefferson RA, Kavanagh TA, Bevan MW: GUS fusions: b-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).PubMedGoogle Scholar
  16. 16.
    Joyce CM, Villemur R, Snustad DP, Silflow CD: Tubulin gene expression in maize (Zea mays L.). Change in isotype expression along the developmental axis of seedling root. J Mol Biol 101: 1680–1689 (1992).Google Scholar
  17. 17.
    Kopczak SD, Haas NA, Hussey PJ, Silflow CD, Snustad DP: The small genome of Arabidopsis thaliana contains at least six expressed a-tubulin genes. Plant Cell 4: 539–547 (1992).CrossRefPubMedGoogle Scholar
  18. 18.
    Langdale JA: In situ hybridization. In: Freeling M, Walbot V (eds) The Maize Handbook, pp. 165–180. Springer-Verlag, New York (1993).Google Scholar
  19. 19.
    Lloyd CW: Cytoskeletal elements of the phragmoplast establish the division plane in vacuolated higher plant cells. In: Lloyd C (ed) The Cytoskeletal Bases of Plant growth and Form, pp. 29–43. Academic Press, London (1991).Google Scholar
  20. 20.
    Montoliu L, Puigdomènech P, Rigau J: The tua3 gene from Z. mays: structure and expression in dividing plant tissues. Gene 94: 201–207 (1990).CrossRefPubMedGoogle Scholar
  21. 21.
    Montoliu L, Rigau J, Puigdomènech P: A tandem of a-tubulin genes preferentially expressed in radicular tissues of Z. mays. Plant Mol Biol 14: 1–15 (1989).CrossRefGoogle Scholar
  22. 22.
    Montoliu L, Rigau J, Puigdomènech P: Analysis by PCR of the number of homologous genomic sequences to a-tubulin in maize. Plant Sci 84: 179–185 (1992).CrossRefGoogle Scholar
  23. 23.
    Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497 (1962).Google Scholar
  24. 24.
    Paszkowski J, Saul MW: Direct gene transfer to plants. Meth Enzymol 118: 668–684 (1986).Google Scholar
  25. 25.
    Rigau J, Capellades M, Montoliu L, Torres MA, Martínez-Izquierdo JA, Tagu D, Puigdomènech P: Analysis of a maize a-tubulin gene promoter by transient expression and in transgenic tobacco plants. Plant J 4: 1043–1050 (1993).Google Scholar
  26. 26.
    Snustad DP, Haas NA, Kopczak SD, Silflow CD: The small genome of Arabidopsis thaliana contains at least nine expressed b-tubulin genes. Plant Cell 4: 549–556 (1992).CrossRefPubMedGoogle Scholar
  27. 27.
    Steeves TA, Sussex IM: Patterns in plant development. Cambridge University Press, Cambridge, UK (1989).Google Scholar
  28. 28.
    Villemur R, Joyce CM, Haas NA, Goddard RH, Kopczak SD, Hussey PJ, Snustad DP, Silflow CD: a-tubulin gene family of maize (Zea mays L.). Evidence for two ancient a-tubulin genes in plants. J Mol Biol 227: 81–96 (1992).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Xavier Uribe
    • 2
  • Miguel Angel Torres
    • 3
  • Montserrat Capellades
    • 1
  • Pere Puigdomènech
    • 1
  • Joan Rigau
    • 1
  1. 1.Departament de Genètica Molecular. Centre d'Investigació i DesenvolupamentConsejo Superior de Investigaciones CientíficasBarcelonaSpain;
  2. 2.Dept. Biología, UAMMadridSpain
  3. 3.Sainsbury LaboratoryNorwichUK

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