Abstract
In the “regeneration” of a shoot from a leaf of the succulent, Graptopetalum paraguayense E. Walther the first new organs are leaf primordia. The original arrangement of cellulose microfibrils and of microtubules (MTs) in the epidermis of the leaf-forming site is one of parallel, straight lines. In the new primordium both structures still have a congruent arrangement but it is roughly in the form of concentric circles that surround the new cylindrical organ. The regions which undergo the greatest shift in orientation (90°) were studied in detail. Departures from the original cellulose alignment are detected in changes in the polarized-light image. Departures from the original cortical MT arrangement are detected using electron microscopy. The over-all reorganization of the MT pattern is followed by the tally of MT profiles, the various regions being studied in two perpendicular planes of section. This corrects for the difference in efficiency in counting transverse versus longitudinal profiles of MTs. Reorientation takes place sporadically, cell by cell, for both the cellulose microfibrils and the MTs, indicating a coordinated reorientation of the two structures. That MTs and cellulose microfibrils reorient jointly in individual cells was shown by reconstruction of the arrays of cortical MTs in paradermal sections of individual cells whose recent change in the orientation of cellulose deposition had been detected with polarized light. Closeness of the two alignments was also indicated by images where the MT and microfibril alignments co-varied within a single cell. The change-over in alignment of the MTs appears to involve stages where arrays of contrasting orientation co-exist to give a criss-cross image. During this critical reorganization, the frequency of the MTs is high. It falls during subsequent enlargement of the organ. It was found that the rearrangement of the cortical MTs to approximate a series of concentric circles on the residual meristem occurred before the emergence of leaf primordia. Through their apparent influence on microfibril alignments, the changes in MT disposition, described here, have the potential to generate major biophysical changes that accompany organogenesis.
Similar content being viewed by others
Abbreviations
- MT(s):
-
microtubule(s)
References
Brennan, J.R. (1970) Colchicine induced microtubule degradation: The basis of C-tumor formation in Phleum pratense. Phytomorphology 20, 309–315
Chafe, S.C., Wardrop, A.B. (1970) Microfibril orientation in plant cell walls. Planta 92, 13–24
Cox, G., Juniper, B. (1973) Electron microscopy of cellulose in entire tissue. J. Microsc. (Oxford) 97, 343–355
Frey-Wyssling, A. (1959) Die pflanzliche Zellwand. Springer, Berlin Göttingen Heidelberg New York
Green, P.B. (1962) Mechanism for plant cellular morphogenesis. Science 138, 1404–1405
Green, P.B. (1980) Organogenesis — a biophysical view. Annu. Rev. Plant Physiol., in press
Green, P.B., Brooks, K.E. (1978) Stem formation from a succulent leaf: Its bearing on theories of axiation. Am. J. Bot. 65, 13–26
Green, P.B., Erickson, R.O., Richmond, P.A. (1970) On the physical basis of cell morphogenesis. Ann. N.Y. Acad. Sci. 175, 712–731
Grimm, I., Sachs, H., Robinson, D.G. (1976) Structure, synthesis and orientation of microfibrils. II. The effect of colchicine on the wall of Oocystis solitaria. Cytobiologie 14, 61–74
Gunning, B.E.S. (1979) Nature and development of microtubule arrays in cells of higher plants. Proc. Electron Microscopy Soc. Am., 37th Meeting, pp. 172–175, Bailey, C.W. ed. Claitors' Publ. Div., Baton Rouge La.
Gunning, B.E.S., Hardham, A.R., Hughes, J.E. (1978a) Pre-prophase bands of microtubules in all categories of formative and proliferative cell division in Azolla roots. Planta 143, 145–160
Gunning, B.E.S., Hardham, A.R., Hughes, J.E. (1978b) Evidence for initiation of microtubules in discrete regions of the cell cortex in Azolla root-tip cells, and an hypothesis on the development of cortical arrays of microtubules. Planta 143, 161–179
Hardham, A.R. (1978) Microtubules and morphogenesis in Azolla pinnata roots. PhD Thesis. The Australian National University, Canberra, Australia
Hardham, A.R., Gunning, B.E.S. (1978a) The structure of cortical microtubule arrays in plant cells. J. Cell Biol. 77, 14–34
Hardham, A.R., Gunning, B.E.S. (1978b) Structure and development of cortical microtubule arrays in plant cells. In: Electron microscopy 1978, 9th Int. Cong. Electron Microscopy Toronto Ont. Canada pp. 264–265, Sturgess, J.M., ed. Microsc. Soc. Canada
Hardham, A.R., Gunning, B.E.S. (1979) Interpolation of microtubules into cortical arrays during cell elongation and differentiation in roots of Azolla pinnata. J. Cell Sci. 37, 411–442
Heath, I.B. (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J. Theor. Biol. 48, 445–449
Hepler, P.K., Fosket, D.F. (1971) The role of microtubules in vessel member differentiation in Coleus. Protoplasma 72, 213–236
Hepler, P.K., Palevitz, B.A. (1974) Microtubules and microfilaments. Annu. Rev. Plant Physiol. 25, 309–362
Hogetsu, T., Shibaoka, H. (1978a) The change of pattern in microfibril arrangement on the inner surface of the cell wall of Closterium acerosum during cell growth. Planta 140, 7–14
Hogetsu, T. Shibaoka, H. (1978b) Effects of colchicine on cell shape and on microfibril arrangement in the cell wall of Closterium acerosum. Planta 140, 15–18
Ledbetter, M.C., Porter, K.R. (1963) A “microtubule” in plant fine structure. J. Cell Biol. 19, 239–250
Maupin-Szamier, P., Pollard, T.D. (1978) Actin filament destruction by osmium tetroxide. J. Cell Biol. 77, 837–852
Newcomb, E.H., Bonnett, H.T., Jr. (1965) Cytoplasmic microtubule and wall microfibril orientation in root hairs of radish. J. Cell Biol. 27, 575–589
O'Brien, T.P. (1972) The cytology of cell wall formation in some eukaryotic cells. Bot. Rev. 38, 87–118
Palevitz, B.A., Hepler, P.K. (1976) Cellulose microfibril orientation and cell shaping in developing guard cells of Allium. The role of microtubules and ion accumulation. Planta 132, 71–93
Pickett-Heaps, J.D., Fowke, L.C. (1970) Mitosis, cytokinesis, and cell elongation in the desmid. Closterium littorale. J. Phycol. 6, 189–215
Robinson, D.G., Grimm, I., Sachs, H. (1976) Colchicine and microfibril orientation. Protoplasma 89, 375–380
Sachs, H., Grimm, I., Robinson, D.G. (1976) Structure, synthesis and orientation of microfibrils. I. Architecture and development of the wall of Oocystis solitaria. Cytobiologie 14, 49–60
Sawhney, V.K., Srivastava, L.M. (1975) Wall fibrils and microtubules in normal and gibberellic-acid-induced growth of lettuce hypocotyl cells. Can. J. Bot. 53, 824–835
Schnepf, E. (1972) The arrangement of microtubules after cell division in young Sphagnum leaflets. Naturwissenschaften 59, 471
Seagull, R.W. (1978) Arrangement of microtubules and microfilaments during oriented secondary wall formation. In: Electron microscopy 1978, 9th Int. Cong. Electron Microscopy, Toronto Ont. Canada, pp. 262–263. Micros. Soc. Canada
Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43
Sutherland, J., McCully, M.E. (1976) A note on the structura changes in the walls of pericycle cells initiating lateral root meristems in Zea mays. Can. J. Bot. 54, 2083–2087
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hardham, A.R., Green, P.B. & Lang, J.M. Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense . Planta 149, 181–195 (1980). https://doi.org/10.1007/BF00380881
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00380881