Abstract
Although the microtubular cytoskeleton of plant cells is important in maintaining the direction of cell growth, its natural lability can be harnessed in such a way that new growth axes are permitted. In these circumstances, the system which fabricates the cytoskeleton is presumably responsive to morphogenetic information originating from outside the cell. Spatial patterns of hormonal and metabolic signals within the tissue or organ that house the responsive cells are one possible source of this information. However, a contrasting source takes the form of biophysical information, such as the supracellular patterns of stresses and strains.
We examined the microtubular cytoskeleton in roots of tomato and maize to test the assumption that the cortical microtubular array of each cell would have a particular orientation relative to the cell's position within the growth field of the root apex. Accordingly, each intracellular cortical array was mapped to the overall pattern of cells within the apex. In certain areas of the meristem, the arrays seemed to be more variable than elsewhere. These are sites where morphogenetic decisions are taken, usually involving a change in the plane of cell division. Roots which have suffered disturbance to their physical structure (e.g. removal of the root cap), or which had been exposed to low temperatures or treated with certain chemicals (e.g. inhibitors of nuclear division or DNA synthesis), exhibited new patterns of microtubular arrays which in turn predicted novel patterns of cell division. In all these circumstances, the arrays showed consistent alterations within distinct regions of the root-e.g. in the quiescent centre and also in a group of cells just behind the quiescent centre, at the boundary between cortex and stele. These altered arrays indicate that there are supracellular domains in which the microtubules respond to morphogenetic signals. Studies such as these reinforce the concept of microtubule lability and the inherent responsiveness of the microtubular system to external and internal stimuli. However, at present there is no indication of how the morphogenetic programme of the root is set up in the first place. Probably, this is established and stabilized early in embryogenesis and is then perpetuated by the prevailing metabolic and biophysical conditions. The microtubules of the cytoskeleton can be regarded as intracellular automata which not only participate in mitosis and cytokinesis but also ensure the realization of an organogenetic programme. Should the root confront circumstances which temporarily destabilize this programme, the prevailing growth field is sufficiently robust to ensure that the microtubular system is attracted back to the stable, pre-existing state capable of reinstating normal morphogenesis. H Lambers Section editor
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akashi T and Shibaoka H 1991 Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J. Cell Sci. 98, 169–174.
Baluška F and Barlow P W 1993 The role of the microtubular cytoskeleton in determining nuclear chromatin structure and passage of maize root cells through the cell cycle. Eur J. Cell Biol. 61, 160–167.
Baluška F, Parker J S and Barlow P W 1992 Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J. Cell Sci. 103, 191–200.
Baluška F, Barlow P W, Hauskrecht M, Kubica Š, Parker J S and Volkmann D 1995 Microtubule arrays in maize root cells. Interplay between the cytoskeleton, nuclear organization and postmitotic cellular growth patterns. New Phytol. 130, 177–192.
Baluška F, Barlow P W, Parker J S and Volkmann D 1996a Reorganization of the radiating endoplasmic microtubules surrounding pre-mitotic and post-mitotic nuclei of cells within a root meristem. J. Plant Physiol. (In press).
Baluška F, Volkmann D, Hauskrecht M and Barlow P W 1996b Auxin-mediated rearrangements of the microtubular cytoskeleton in growing maize root cells: Rapid disintegration versus reorientation of cortical microtubules. Plant Cell Physiol. (In press).
Baluška F, Vitha S, Barlow P W and Volkmann D 1996c Rearrangements of F-actin arrays in cells of intact maize root apex tissues: A major developmental switch occurs in the postmitotic region. Eur. J. Cell Biol. (In press).
Barlow P W 1974 Regeneration of the cap of primary roots ofZea mays. New Phytol. 73, 937–954.
Barlow P W 1987 The hierarchical organization of plants and the transfer of information during their development. Postepy Biol. Komork. 14, 63–82.
Barlow P W 1993a Review of the cytoskeletal basis of plant growth and form. Plant Growth Regul. 13, 122–123.
Barlow P W 1993b The cell division cycle in relation to root organogenesis.In Molecular and Cell Biology of the Plant Cell Cycle. Eds. DFrancis and J COrmrod. pp 179–199. Kluwer Acad. Publ., Dordrecht, the Netherlands.
Barlow P W 1994 Cell division in meristems and their contribution to organogenesis and plant form.In Shape and Form in Plants and Fungi. Eds. D SIngram and AHudson. pp 169–193. Academic Press, London, UK.
Barlow P W 1995 The cytoskeleton and its role in determining the cellular architecture of roots. Giorn. Bot. Ital. 129, 863–872.
Barlow P W 1996 Cellular patterning in root meristems: its origins and significance.In Plant Roots. The Hidden Half. 2nd ed. Eds. YWaisel, AEshel and UKafkafi. pp 77–109. Marcel Dekker, New York, USA.
Baskin T I and Cande W Z 1990 The structure and function of the mitotic spindle in flowering plants. Annu. Rev. Plant Physiol. Plant Molec. Biol. 41, 277–315.
Blancaflor E B and Hasenstein K H 1995 Time course and auxin sensitivity of cortical microtubule reorientation in maize roots. Protoplasma. 185, 72–82.
Cyr R J 1994 Microtubules in plant morphogenesis: Role of the cortical array. Annu. Rev. Cell Biol. 10, 153–180.
Edelman H G and Sievers A 1995 Unequal distribution of osmiophilic particles in the epidermal periplasmic space of upper and lower flanks of gravi-responding rye coleoptiles. Planta 196, 396–399.
Giddings T HJr and Staehelin L A 1991 Microtubule-mediated control of microfibril deposition: A re-examination of the hypothesis.In The Cytoskeletal Basis of Plant Growth and Form. Ed. C WLloyd. pp. 85–99. Academic Press, London, UK.
Goethe J Wvon 1790 Versuch die Metamorphose der Pflanzen zu 093 erklären. Ettinger, Gotha, Germany.
Green P B 1962 Mechanisms for plant cellular morphogenesis. Science 138, 1404–1405.
Green P B and Selker J M L 1991 Mutual alignments of cell walls, cellulose, and cytoskeletons: their role in meristems.In The Cytoskeletal Basis of Plant Growth and Form. Ed. C WLloyd. pp 303–322. Academic Press, London, UK.
Hay A and Mabberley D J 1994 On perception of plant morphology: Some implications for phylogeny.In Shape and Form in Plants and Fungi. Eds. D SIngram and AHudson. pp 101–117. Academic Press, London, UK.
Ishida K and Katsumi M 1992 Effects of gibberellin and abscisic acid on the cortical microtubule orientation in hypocotyl cells of light-grown cucumber seedlings. Int. J. Plant Sci. 153, 155–163.
Lambert A-M 1993 Microtubule-organizing centres in higher plant cells. Curr. Opinion Cell Biol. 5, 116–122.
Ledbetter M C and Porter K R 1963 A “microtubule” in plant cell fine structure. J. Cell Biol. 19, 239–250.
Mazia D 1987 The chromosome cycle and the centrosome cycle in the mitotic cycle. Int. Rev. Cytol. 100, 49–92.
Mazia D 1993 The cell cycle at the cellular level. Eur. J. Cell Biol. 61, 14.
Smith-Huerta N L and Jernstedt J A 1989 Root contraction in hyacinth. III. Orientation of cortical microtubules visualized by immunofluorescence microscopy. Protoplasma 151, 1–10.
Stoppin V, Vantard M, Schmidt A-C and Lambert A-M 1994 Isolated plant nuclei nucleate microtubule assembly: The nuclear surface in higher plants has centrosome-like activity. Plant Cell 6, 1099–1106.
Van'tHof J and Lamm S S 1992 Site of initiation of replication of the ribosomal genes of pea (Pisum sativum) detected by twodimensional gel electrophoresis. Plant Mol. Biol. 20, 377–382.
Wick S M 1991 The preprophase band.In The Cytoskeletal Basis of Plant Growth and Form. Ed. C WLloyd. pp 231–244. Academic Press, London, UK.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Barlow, P.W., Parker, J.S. Microtubular cytoskeleton and root morphogenesis. Plant Soil 187, 23–36 (1996). https://doi.org/10.1007/BF00011654
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00011654