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Mechanism for formation of the secondary wall thickening in tracheary elements: Microtubules and microfibrils of tracheary elements of Pisum sativum L. and Commelina communis L. and the effects of amiprophosmethyl

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Abstract

Arrangements of microfibrils (MFs) and microtubules (MTs) were examined in tracheary elements (TEs) of Pisum sativum L. and Commelina communis L. by production of replicas of cryo-sections, and by immunofluorescence microscopy, respectively. The secondary wall thickenings of TEs of Pisum and Commelina roots have pitted and latticed patterns, respectively. Most MFs in the pitted thickening of Pisum TEs retain a parallel alignment as they pass around the periphery of pits. However, some groups of MFs grow into the pits but then terminate at the edge of the thickening, indicating that cellulose-synthase complexes are inactivated in the plasma membrane under the pit. Microtubules of TEs of both Pisum and Commelina are localized under the secondary thickening and few MTs are detected in the areas between wall thickenings. In the presence of the MT-disrupting agent, amiprophosmethyl, cellulose and hemicellulose, which is specific to secondary thickening, are deposited in deformed patterns in TEs of Pisum roots, Pisum epicotyls and Commelina roots. This indicates that the localized deposition of hemicellulose as well as cellulose involves MTs. The deformed, but heterogeneous pattern of secondary thickening is still visible, indicating that MTs are involved in determining and maintaining the regular patterns of the secondary thickening but not the spatial heterogeneous pattern of the wall deposition. A working hypothesis for the formation of the secondary thickening is proposed.

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Abbreviations

APM:

amiprophosmethyl

DMSO:

dimethyl sulfoxide

F-WGA:

fluorescein-conjugated wheat-germ agglutinin

M F:

microfibril

MT:

microtubule

PEG:

polyethyleneglycol

TE:

tracheary element

References

  1. Dute, R.R., Rushing, A.E. (1988) Notes on torus development in the wood of Osmanthus americanus (L.) Benth. & Hook. ex Gray (Oleaceae). IAWA Bull. n.s. 9, 41–51

  2. Dute, R.R., Rushing, A.E., Perry, J.W. (1990) Torus structure and development in species of Daphne. IAWA Bull. n.s. 11, 401–412

  3. Giddings, T.H., Brower, D.L., Staehelin, L.A. (1980) Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. J. Cell Biol. 84, 327–339

  4. Hardham, A.R. (1982) Regulation of polarity in tissues and organs. In: The cytoskeleton in plant growth and development, pp. 377–403, Lloyd, C.W., ed. Academic Press, London

  5. Hardham, A.R., Gunning, B.S.A. (1979) Interpolation of microtubules into cortical arrays during cell elongation and differentiation in roots of Azolla pinnata. J. Cell Sci. 37, 411–442

  6. Hepler, P.K., Fosket, D.F. (1971) The role of microtubules in vessel member differentiation in Coleus. Protoplasma 72, 213–236

  7. Hepler, P.K., Newcomb, E.H. (1964) Microtubules and fibrils in the cytoplasm of Coleus cells undergoing secondary wall deposition. J. Cell Biol. 20, 529–533

  8. Hepler, P.K., Palevitz, B.A. (1974) Microtubules and microfilaments. Annu. Rev. Plant Physiol. 25, 309–362

  9. Herth, W. (1985) Plasma membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164, 12–21

  10. Hogetsu, T. (1983) Distribution and local activity of particle complexes synthesizing cellulose microfibrils in the plasma membrane of Closterium acerosum (Schrank) Ehrenberg. Plant Cell Physiol. 24, 777–781

  11. Hogetsu, T. (1986) Re-formation of microtubules in Closterium ehrenbergii Meneghini after cold-induced depolymerization. Planta 167, 437–443

  12. Hogetsu, T. (1989) The arrangement of microtubules in leaves of monocotyledonous and dicotyledonous plants. Can. J. Bot. 67, 3506–3512

  13. Hogetsu, T. (1990) Detection of hemicelluloses specific to the cell wall of tracheary elements and phloem cells by fluorescein-conjugated lectins. Protoplasma 156, 67–73

  14. Hogetsu, T., Oshima, Y. (1985) Immunofluorescence microscopy of microtubule arrangement in Closterium acerosum (Schrank) Ehrenberg. Planta 166, 169–175

  15. Hogetsu, T., Oshima, Y. (1986) Immunofluorescence microscopy of microtubule arrangement in root cells of Pisum sativum L. var Alaska. Plant Cell Physiol. 27, 939–945

  16. Hogetsu, T., Takeuchi, Y. (1982) Temporal and spatial changes of cellulose synthesis in Closterium acerosum (Schrank) Ehrenberg during cell growth. Planta 154, 426–434

  17. Inoué, T., Osatake, H. (1988) A new drying method of biological specimens for scanning electron microscopy: the t-butyl alcohol freeze-drying method. Arch. Histol. Cytol. 51, 53–59

  18. Keller, B., Templeton, M.D., Lamb, C.J. (1989) Specific localization of a plant cell wall glycine-rich protein in protoxylem cells of the vascular system. Proc. Natl. Acad. Sci. USA 86, 1529–1533

  19. Ledbetter, M.C., Porter, K.R. (1963) A “microtubule” in plant cell fine structure. J. Cell Biol. 19, 239–250

  20. Moore, P.J., Staehelin, L.A. (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.; implication for secretory pathways. Planta 174, 433–445

  21. Northcote, D.H. (1963) The biology and chemistry of the cell walls of higher plants, algae and fungi. Int. Rev. Cytol. 14, 223–265

  22. Northcote, D.H. (1989) Control of plant cell wall biogenesis: an overview. In: Plant cell wall polymers. Biogenesis and biodegradation (ACS symposium series 399), pp. 1–15, Lewis, N.G., Paice, M.G., eds. Am. Chem. Soc., Washington DC

  23. Northcote, D.H., Davey, R., Lay, J. (1989) Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary walls of plant cells. Planta 178, 353–366

  24. Pickett-Heaps, J.D. (1967) The effects of colchicine on the ultrastructure of dividing plant cells, xylem wall differentiation and distribution of cytoplasmic microtubules. Devel. Biol. 15, 206–236

  25. Schneider, B., Herth, W. (1986) Distribution of plasma membrane rosettes and kinetics of cellulose formation in xylem development of higher plants. Protoplasma 131, 142–152

  26. Staehelin, L.A., Giddings, T.H. (1982) Membrane-mediated control of cell wall microfibrillar order. In: Developmental order: its origin and regulation, pp. 133–147, Subtelny, S., Green, P.B., eds. Alan R. Liss Inc., New York

  27. Wooding, F.B.P., Northcote, D.H. (1964) The development of the secondary wall of the xylem in Acer pseudoplatanus. J. Cell Biol. 23, 327–337

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Additional information

I thank Ms. Aiko Hirata (Institute of Applied Microbiology, University of Tokyo, Japan) for help in taking stereomicrographs. This work was supported in part by a Grant-in-Aid from the Ministry of Education, Science and Culture of Japan.

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Hogetsu, T. Mechanism for formation of the secondary wall thickening in tracheary elements: Microtubules and microfibrils of tracheary elements of Pisum sativum L. and Commelina communis L. and the effects of amiprophosmethyl. Planta 185, 190–200 (1991). https://doi.org/10.1007/BF00194060

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Key words

  • Amiprophosmethyl
  • Commelina
  • Microfibril
  • Microtubule
  • Pisum (secondary wall thickening)
  • Secondary wall thickening
  • Tracheary element