Skip to main content
Log in

β-glucuronidase as a marker for clonal analysis of tomato lateral roots

  • Papers
  • Published:
Transgenic Research Aims and scope Submit manuscript

Abstract

In higher plants, the root-shoot axis established during embryogenesis is extended and modified by the development of primary and lateral apical meristems. While the structure of several shoot apical meristems has been deduced by combining histological studies with clonal analysis, the application of this approach to root apical meristems has been limited by a lack of visible genetic markers. We have tested the feasibility of using a synthetic gene consisting of the maize transposable elementActivator (Ac) inserted between a 35S CaMV promoter and the coding region of a β-glucuronidase (GUS) reporter gene as a means of marking cell lineages in roots. The GUS gene was activated in individual cells byAc excision, and the resulting sectors of GUS-expressing cells were detected with the histochemical stain X-Gluc. Sectors in lateral roots originated from bothAc excision in meristematic cells and from parent root sectors that bisect the founder cell population for the lateral root initial. Analysis of root tip sectors confirmed that the root cap, and root proper have separate initials. Large sectors in the body of the lateral root encompassed both cortex and vascular tissues. The number of primary initial cells predicted from the size and arrangement of the sectors observed ranged from two to four and appeared to vary between roots. We conclude that transposon-based clonal analysis using GUS expression as a genetic marker is an effective approach for deducing the functional organization of root apical meristems.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barlow, P. W. (1976) Towards an understanding of the behaviour of root meristems.J. Theor. Biol. 57, 433–51.

    Google Scholar 

  • Barlow, P. W. (1987) Cellular packets, cell division and morphogenesis in the primary root meristem ofZea mays L.New Phytol. 105, 27–56.

    Google Scholar 

  • Blakely, L. M., Durham, M., Evans, T. A. and Blakely, R. M. (1982) Experimental studies on lateral root formation in radish seedling roots. I. General methods, developmental stages, and spontaneous formation of laterals.Bot. Gaz. 143, 341–52.

    Google Scholar 

  • Brumfield, R. T. (1943) Cell lineage studies in root meristems by means of chromosome rearrangements induced by X-rays.Amer. J. Bot. 30, 101–10.

    Google Scholar 

  • Byrne, J. M., Byrne, J. M. and Emmitt, D. P. (1982) Development and structure of the vascular connection between the primary and lateral root ofLycopersicon esculentum.Amer. J. Bot. 69, 287–97.

    Google Scholar 

  • Clowes, F. A. L. (1981) The difference between open and closed meristems.Ann. Bot. 48, 761–7.

    Google Scholar 

  • Clowes, F. A. L. (1984) Size and activity of quiescent centres of roots.New Phytol. 96, 13–21.

    Google Scholar 

  • Dawe, R. K. and Freeling, M. (1991) Cell lineage and its consequences in higher plants.Plant J. 1, 3–8.

    Google Scholar 

  • Dietrich, R. A., Radke, S. E. and Harada, J. J. (1992) Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings.Pl. Cell. 4, 1371–82.

    Google Scholar 

  • Dulieu, H. (1965) Reactions morphologiques des plantules deNicotiana tabacum L. et deNicotiana glutinosa L. au traitement des graines par le methane sulfonate d'ethyle. Consequences sur l'apparition de mutations chlorophylliennes somatiques.Ann. Amelior. Plant. 15, 359–72.

    Google Scholar 

  • Dulieu, H. (1969) Mutations somatiques chlorophylliennes induites et ontogenie caulinaire.Bull. Sci. Bourgogne 26, 1–84.

    Google Scholar 

  • Fillatti, J. J., Kiser, J., Rose, R. and Comai, L. (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binaryAgrobacterium tumefaciens vector.Bio/Technology 5, 726–30.

    Google Scholar 

  • Finnegan, E. J., Taylor, B. H., Craig, S. and Dennis, E. S. (1989) Transposable elements can be used to study cell lineages in transgenic plants.Pl. Cell 1, 757–64.

    Google Scholar 

  • Furner, I. J. and Pumfrey, J. E. (1992) Cell fate in the shoot meristem ofArabidopsis thaliana.Development 115, 755–64.

    Google Scholar 

  • Greenblatt, I. M. (1984) A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element,Modulator, in maize.Genetics 108, 471–85.

    Google Scholar 

  • Gutierrez, R. G., Carroll, R. J., Wang, N., Lee, G. H. and Taylor, B. H. Analysis of tomato root initiation using a normal mixture distribution. Manuscript submitted.

  • Irish, V. F. (1991) Cell lineage in plant development.Current Opinions in Genetics and Development 1, 169–71.

    Google Scholar 

  • Irish, V. F. and Sussex, I. M. (1992) A fate map of theArabidopsis embryonic shoot apical meristem.Development 115, 745–53.

    Google Scholar 

  • Jefferson, R. A., Kavanaugh, T. A. and Bevan, M. W. (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.EMBO J. 6, 3901–7.

    Google Scholar 

  • Jegla, D. E. and Sussex, I. M. (1989) Cell lineage patterns in the shoot meristem of the sunflower embryo in the dry seed.Dev. Biol. 131, 215–25.

    Google Scholar 

  • Lyndon, R. F. (1990)Plant Development — The Cellular Basis. pp. 19–57. London: Unwin Hyman.

    Google Scholar 

  • MacLeod, R. D. (1991) The root apical meristem and its margins. In: Waisel, Y., Eshel, A. and Kafkafi, U. (eds).Plant Roots: the Hidden Half, pp. 75–101. New York: Marcel Dekker.

    Google Scholar 

  • McDaniel, C. N. and Poethig, R. S. (1988) Cell-lineage patterns in the shoot apical meristem of the germinating maize embryo.Planta 175, 13–22.

    Google Scholar 

  • McFadden, G. I., Bonig, I., Cornish, E. C. and Clarke, A. E. (1988) A simple fixation and embedding method for use in hybridization histochemistry on plant tissues.Histochem. J. 20, 575–86.

    Google Scholar 

  • Poethig, R. S. (1987) Clonal analysis of cell lineage patterns in plant development.Amer. J. Bot. 74, 581–94.

    Google Scholar 

  • Poethig, R. S. (1989) Genetic mosaics and cell lineage analysis in plants.Trends in Genetics 5, 273–7.

    Google Scholar 

  • Poethig, R. S., Coe, E. S. and Johri, M. M. (1986) Cell lineage patterns in maize embryogenesis: a clonal analysis.Dev. Biol. 117, 392–404.

    Google Scholar 

  • Ruth, J., Klekowski, E. J. and Stein, O. L. (1985) Impermanent initials of the shoot apex and diplontic selection in a juniper chimera.Amer. J. Bot. 72, 1127–35.

    Google Scholar 

  • Seago, J. L. (1973) Developmental anatomy in roots ofIpomoea purpurea. II. Initiation and development of secondary roots.Amer. J. Bot. 60, 607–18.

    Google Scholar 

  • Steeves, T. A. and Sussex, I. M. (1989)Patterns in Plant Development, pp. 203–53. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Street, H. E. and McGregor, S. M. (1952) The carbohydrate nutrition of tomato roots. III. The effect of external sucrose concentration on the growth and anatomy of excised roots.Ann. Bot. 16, 185–205.

    Google Scholar 

  • Street, H. E., Opik, H. and James, F. E. L. (1967) Fine structure of the main axis meristems of cultured tomato roots.Phytomorphology 17, 391–401.

    Google Scholar 

  • Taylor, B. H. and Scheuring, C. F. (1990) The maize transposable element Ac exhibits variable activity in transgenic tomato.Tomato Genetics Cooperative Report 40, 37–8.

    Google Scholar 

  • Terryn, N., Arias, M. B., Engler, G., Tiré, C., Villaroel, R., Van Montagu, M. and Inzé, D. (1993)rha1, a gene encoding a small GTP binding protein fromArabidopsis, is excressed primarily in developing guard cells.Pl. Cell 5, 1761–9.

    Google Scholar 

  • Tilney-Bassett, R. A. E. (1986)Plant Chimeras. London: Edward Arnold.

    Google Scholar 

  • Webster, P. L. and McLeod, R. D. (1980) Characteristics of root apical meristem cell population kinetics: a review of analyses and concepts.Envir. Exp. Bot. 20, 335–58.

    Google Scholar 

  • White, P. R. (1934) Potentially unlimited growth of excised tomato root tips in a liquid medium.Pl. Physiol. 9, 585–600.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, GH., Rodgers, L. & Taylor, B.H. β-glucuronidase as a marker for clonal analysis of tomato lateral roots. Transgenic Research 4, 123–131 (1995). https://doi.org/10.1007/BF01969414

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01969414

Keywords

Navigation