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.
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.
Barlow, P. W. (1987) Cellular packets, cell division and morphogenesis in the primary root meristem ofZea mays L.New Phytol. 105, 27–56.
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.
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.
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.
Clowes, F. A. L. (1981) The difference between open and closed meristems.Ann. Bot. 48, 761–7.
Clowes, F. A. L. (1984) Size and activity of quiescent centres of roots.New Phytol. 96, 13–21.
Dawe, R. K. and Freeling, M. (1991) Cell lineage and its consequences in higher plants.Plant J. 1, 3–8.
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.
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.
Dulieu, H. (1969) Mutations somatiques chlorophylliennes induites et ontogenie caulinaire.Bull. Sci. Bourgogne 26, 1–84.
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.
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.
Furner, I. J. and Pumfrey, J. E. (1992) Cell fate in the shoot meristem ofArabidopsis thaliana.Development 115, 755–64.
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.
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.
Irish, V. F. and Sussex, I. M. (1992) A fate map of theArabidopsis embryonic shoot apical meristem.Development 115, 745–53.
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.
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.
Lyndon, R. F. (1990)Plant Development — The Cellular Basis. pp. 19–57. London: Unwin Hyman.
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.
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.
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.
Poethig, R. S. (1987) Clonal analysis of cell lineage patterns in plant development.Amer. J. Bot. 74, 581–94.
Poethig, R. S. (1989) Genetic mosaics and cell lineage analysis in plants.Trends in Genetics 5, 273–7.
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.
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.
Seago, J. L. (1973) Developmental anatomy in roots ofIpomoea purpurea. II. Initiation and development of secondary roots.Amer. J. Bot. 60, 607–18.
Steeves, T. A. and Sussex, I. M. (1989)Patterns in Plant Development, pp. 203–53. Cambridge, UK: Cambridge University Press.
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.
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.
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.
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.
Tilney-Bassett, R. A. E. (1986)Plant Chimeras. London: Edward Arnold.
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.
White, P. R. (1934) Potentially unlimited growth of excised tomato root tips in a liquid medium.Pl. Physiol. 9, 585–600.
Author information
Authors and Affiliations
Rights 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
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01969414