Abstract
Evidence is presented which supports the concept of a functional membrane barrier in the transition zone at the base of each flagellum of Chlamydomonas eugametos gametes. This makes it unlikely that agglutination factors present on the surface of the cell body can diffuse or be transported to the flagellar membrane. The evidence is as follows: 1) The glycoprotein composition of the flagellar membrane is very different to that of the cell-body plasma membrane. 2) The flagella of gametes treated with cycloheximide, tunicamycin or α, α′-dipyridyl become non-agglutinable but the source of agglutination factors on the cell body is not affected. 3) Even under natural conditions when the flagella are non-agglutinable, for example in vis-à-vis pairs or in appropriate cell strains that are non-agglutinable in the dark, the cell bodies maintain the normal complement of active agglutinins. 4) When flagella of living cells are labeled with antibodies bound to fluorescein, the label does not diffuse onto the cell-body surface. 5) When gametes fuse to form vis-à-vis pairs, the original mating-type-specific antigenicity of each cell body is slowly lost (probably due to the antigens diffusing over both cell bodies), while the specific antigenicity of the flagellar surface is maintained. Even when the flagella of vis-à-vis pairs are regenerated from cell bodies with mixed antigenicity, the antigenicity of the flagella remains matingtype-specific. 6) Evidence is presented for the existence of a pool of agglutination factors within the cell bodies but not on the outer surface of the cells.
Similar content being viewed by others
Abbreviations
- CHI:
-
cycloheximide
- GTC:
-
guaniline thiocyanate
- mt +/mt - :
-
mating type plus or minus
- PAS:
-
Periodic-acid-Schiff reagent
- SDS:
-
sodium dodecyl sulphate
References
Bouck, G.B., Chen, S.J. (1984) Synthesis and assembly of the flagellar surface. J. Protozool. 31, 21–24
Bray, D.F., Nakamura, K., Wagenaar, E.B. (1983) Spiral arrays: novel intramembranous particle arrays of the plasma membrane of Chlamydomonas eugametos. Micron. Micros. Acta 14, 345–349
Cooper, J.B., Adair, W.S., Mecham, R.P., Heuser, J.E., Goodenough, U.W. (1983) Chlamydomonas agglutinin is a hydroxyproline-rich glycoprotein. Proc. Natl. Acad. Sci. USA 80, 5898–5901
Goodenough, U.W. (1983) Motile detergent-extracted cells of Tetrahymena and Chlamydomonas. J. Cell Biol. 96, 1610–1621
Homan, W.L., Gijsberti Hodenpijl, P., Musgrave, A., van den Ende, H. (1982) Reconstitution of biological activity in isoagglutinins from Chlamydomonas eugametos. Planta 155, 529–535
Klis, F.M., Samson, M.R., Touw, E., Musgrave, A., van den Ende, H. (1985) Sexual agglutination in the unicellular green alga Chlamydomonas eugametos. Identification and properties of the mating type plus agglutination factor. Plant Physiol. 79, 740–745
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680–685
Lens, P.F., van den Briel, M.L., Musgrave, A., van den Ende, H. (1980) Sex-specific glycoproteins in Chlamydomonas flagella. An immunological study. Arch. Microbiol. 126, 77–81
Lens, P.F., Olofsen, F., Nederbragt, A., Musgrave, A., van den Ende, H. (1982) An antiserum against a glycoprotein functional in flagellar adhesion between Chlamydomonas eugametos gametes. Arch. Microbiol. 131, 241–246
Lewin, R.A. (1952) Studies on the flagella of algae. I. General observations on Chlamydomonas moeswusii Gerloff. Biol. Bull. 102, 74–79
Lewin, R.A. (1954) Sex in unicellular algae. In: Sex in microorganisms, pp. 100–133, Washington, D.C. ed. Am. Association for the Advancement of Science, Washington, D.C., USA
Mesland, D.A.M. (1976) Mating in Chlamydomonas eugametos. A scanning electron microscopical study. Arch. Microbiol. 109, 31–35
Moestrup, O. (1982) Flagellar structure in algae: a review, with new observations particularly on the Chrysophyceae, Phaeophyceae (Flucophyceae), Euglenophyceae, and Reckertia. Phycologia 21, 427–528
Monk, B.C., Adair, W.S., Cohen, R.A., Goodenough, U.W. (1983) Topography of Chlamydomonas: fine structure and polypeptide components of the gametic flagellar membrane surface and the cell wall. Planta 158, 517–533
Musgrave, A., van Eijk, E., te Welscher, R., Broekman, R., Lens, P.F., Homan, W.L., van den Ende, H. (1981) Sexual agglutination factor from Chlamydomonas eugametos. Planta 153, 362–369
Musgrave, A., de Wildt, P., Broekman, R., van den Ende, H. (1983) The cell wall of Chlamydomonas eugametos. Immunological aspects. Planta 158, 82–89
Pijst, H.L.A., Zilver, R.J., Musgrave, A., van den Ende, H. (1983) Agglutination factor in the cell body of Chlamydomonas eugametos. Planta 158, 403–409
Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212
Robertson, J.G., Wells, B., Bisseling, T., Farnden, K.J.F., Johnston, A.W.B. (1984) Immuno-gold localization of Leghaemoglobin in cytoplasm in nitrogen-fixing root nodules of pea. Nature 311, 254–256
Snell, W.J., Moore, W.S. (1980) Aggregation dependent turnover of flagellar adhesion molecules in Chamydomonas gametes. J. Cell Biol. 84, 203–210
Solter, K.M., Gibor, A. (1978) Removal and recovery of mating receptors on flagella of Chlamydomonas reinhardtii. Exp. Cell Res. 115, 175–181
Tomson, A.M., Demets, R., Bakker, N.P.M., Stegwee, D., van den Ende, H. (1985) Gametogenesis in liquid cultures of Chlamydomonas eugametos. J. Gen. Microbiol. 131, 1553–1560
Weiss R.L. (1983) Coated vesicles in the contractile vacuole/mating structure region of Chlamydomonas. J. Ultrastruct. Res. 85, 33–44
Weiss, R.L., Goodenough, D.A., Goodenough, U.W. (1977) Membrane particle arrays associated with the basal body and with contractile vacuole secretion in Chlamydomonas. J. Cell Biol. 72, 133–143
Wiese, L., Mayer, R.A. (1982) Unilateral tunicamycin sensitivity of gametogenesis in dioecious isogamous Chlamydomonas species. Gamete Res. 5, 1–9
Witman, G.B.K., Carlson, J., Berliner, J., Rosenbaum, J.L. (1972) Chlamydomonas flagella. I. Isolation and electrophoresic analysis of microtubules, matrix, membranes and mastigonemes. J. Cell Biol. 54, 507–539
Zacharius, R.M., Zell, T.E., Morrison, J.M., Woodlock, J.J. (1969) Glycoprotein staining following electrophoresis on acrylamide gels. Anal. Biochem. 30, 148–152
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Musgrave, A., de Wildt, P., van Etten, I. et al. Evidence for a functional membrane barrier in the transition zone between the flagellum and cell body of Chlamydomonas eugametos gametes. Planta 167, 544–553 (1986). https://doi.org/10.1007/BF00391231
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00391231