Abstract
Using immunocytochemistry combined with light and electron microscopy, antibodies against cotton (Gossypium hirsutum) Ces A3 were used to identify and localize Ces A proteins in Micrasterias denticulata. Silver-enhanced, immuno-gold labeling of Ces A was localized on the plasma membrane with light and immuno-electron microscopy. Immuno-gold labeling of \(\beta\)-1,4-glucan synthase always was observed in contact with the tips of negatively stained cellulose microfibrils. Although the \(\beta\)-1,4-glucan synthesizing system in the cell wall of Micrasterias denticulata has been investigated by several methods in the past few decades, these results provide the first significant evidence that the hexagonal arrays of ‘rosettes’ observed in the freeze-etch replica techniques within the plasma membrane of Micrasterias denticulata are \(\beta\)-1, 4-glucan synthases. In addition, the antibodies to cotton Ces A3 show no reactivity with \(\beta\)-1,4-glucan synthases from Boergesenia forbesii (a Siphonocladaceaen alga with linear terminal complexes=TCs). These results suggest that the specific morphology of TCs (e.g., rosette or linear arrangement) is closely related to the cellulose synthase antibody binding sites (catalytic domains). These data are consistent with a recent phylogenic analysis which shows that Mesotaenium caldariorum possesses Ces A-type genes that are closely related to Ces A’s in vascular plants. This report suggests a significant divergence between the cellulose synthase catalytic subunits of the Chlorophyta (linear TCs) and the Streptophyta (rosette TCs).
Similar content being viewed by others
References
Atalla R.H., VanderHart D.L. (1984). Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285
Bold H.C., Wynne M.J. (1978). Introduction to the Algae: Structure and Reproduction. Prentice Hall, Englewood Cliffs, New Jersey
Brown R.M. Jr. (1996). The biosynthesis of cellulose. J. Macromol. Sci. A 33(10): 345–1373
Dobberstein B., Kiermayer O. (1972). Das Auftreten eines bosonderen Typs von Golgivesikeln warend der Sekundarwandbildung von Micrasterias denticulata Breb. Protoplasma 75:185–194
Drawert H., Mix M. (1962). Zur funktion des Golgi-apparates in der pflanzenzelle. Planta 58: 448–452
Emons A.M.C. (1985). Plasma-membrane rosettes in root hairs of Equisetum hyemale. Planta 163: 350–359
French A.D., Delmer D.P. (1999). The structure and mechanism of biosynthesis of cellulose. In: Kung S.D., Yang S.F. (eds). The Discoveries in Plant Biology Series. Vol. 3. World Sciences, Hong Kong
Giddings T.H., Brown 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 wall. J. Cell Biol. 84:327–329
Hausser I., Herth W. (1983). The Ca2+-chelating antibiotic, chlortetracycline (CTC), disturbs multipolar tip growth and primary wall formation in Micrasterias. Protoplasma 117: 167–173
Hermann S., Gebhard V.J. (1987). Tricine-SDS poly acrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368–379
Imai T., Sugiyama J., Itoh T. and Horii F. 1999. Almost pure I-α cellulose in the cell wall of Glaucocystis. J. Struct. Biol. 127: 248–257
Karol K.G., McCourt R.M., Cimino M.T. and Delwiche C.F. 2001. The closest living relatives of land plants. Science 294: 2351–2353
Kiermayer O. (1968). The distribution of microtubules in differentiating cells of Micrasterias denticulata Breb. Planta 83: 223–236
Kiermayer O., Staehelin L.A. (1972). Feinstruktur von Zellwand und Plasmamembran bei Micrasterias denticulata Breb. nach Gefrieratzung. Protoplasma 74: 227–237
Kiermayer O., Sleytr U.B. (1979). Hexagonally ordered “rosettes” of particles in the plasma membrane of Micrasterias denticulata Breb. and their significance for microfibril formation and orientation. Protoplasma 101: 133–138
Kiermayer O. (1981). Cytoplasmic basis of morphogenesis in Micrasterias. In: Kiermayer O. (eds). Cytomorphogenesis in Plants, Cell Biology Monographs 8. Springer-Verlag, Vienna, New York, pp. 148–189
Kim N.H., Herth W., Vuong W., Chanzy H. (1996). The cellulose system in the cell wall of Micrasterias. J. Struct. Biol. 117: 195–203
Kimura S., Itoh T. (1995). Evidence for the role of the glomerulocyte in cellulose synthesis in the tunicate, Metandrocarpa uedai. Protoplasma 186: 24–33
Kimura S., Laosinchai W., Itoh T., Cui X., Linder R., Brown R.M. Jr. (1999). Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11: 2075–2085
Meindl U.L. (1982). Local accumulation of membrane-associated calcium according to cell pattern formation in Micrasterias denticulata visualized by chlorotetracycline fluorescence. Protoplasma 110:143–146
Meindl U.L., Salomon S.B. (2000). Cell wall secretion in the green alga Micrasterias. J. Microsc. 198: 208–217
Mueller S.C., Brown R.M. Jr. (1980). Evidence for an intramembrane component associated with a cellulose microfibril synthesizing complex in higher plants. J. Cell Biol. 84: 315–326
Nakashima J., Awano T., Takabe K., Fujita M., Saiki H. (1997). Immunocytochemical localization of phenylalanine ammonia-lyase and cinnamyl alcohol dehydrogenase in differentiating tracheary elements derived from Zinnia mesophyll cells. Plant Cell Physiol. 38: 113–123
Nakashima J., Laosinchai W., Cui X., Brown R.M. Jr. (2003). New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 10(4):369–389
Pear J., Kawagoe Y., Schreckengost W., Delmer D.P., Stalker D. (1996). Higher plants contain homologs of the bacterial CelA genes encoding the catalytic subunit of the cellulose synthase. Proc. Natl. Acad. Sci. USA 93: 12637–12642
Roberts A.W., Roberts E.M., Delmer D.P. (2002). Cellulose synthase (Ces A) genes in the green alga Mesotaenium caldariorum. Eukaryot. Cell 1: 847–855
Schnepf E., White O., Rudolph U., Deichgraber G., Reiss H.D. (1985). Tip cell growth and the frequency and distribution of particle rosettes in the plasmalemma: experimental studies of in Funaria protonema cells. Protoplasma 127: 222–229
Sugiyama J., Vuong R., Chanzy H. (1991). Electron diffraction study of two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules 24: 4168–4175
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nakashima, J., Heathman, A. & Brown, R. Antibodies against a Gossypium hirsutum recombinant cellulose synthase (Ces A) specifically label cellulose synthase in Micrasterias denticulata . Cellulose 13, 181–190 (2006). https://doi.org/10.1007/s10570-006-9059-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10570-006-9059-y