Advertisement

Protoplasma

, Volume 194, Issue 1–2, pp 18–28 | Cite as

Thrust reversal by tubular mastigonemes: immunological evidence for a role of mastigonemes in forward motion of zoospores ofPhytophthora cinnamomi

  • David M. Cahill
  • Michele Cope
  • Adrienne R. Hardham
Article

Summary

The role of tubular mastigonemes in the reversal of thrust of the anterior flagellum ofPhytophthora cinnamomi was analysed using mastigoneme-specific monoclonal antibodies and immunoflu-orescence and video microscopy. Exposure of live zoospores ofP. cinnamomi to the mastigoneme-specific Zg antibodies caused alterations in the arrangement of mastigonemes on the flagellar surface and at Zg concentrations above 0.3 μ/ml, mastigonemes became detached from the flagellum. As a consequence of antibody binding to the mastigonemes there were concentration-dependent perturbations in zoospore swimming behaviour and anterior flagellum beat pattern. With increasing antibody concentration zoospores swam more slowly and other parameters of their swimming pattern, such as the wavelength of the swimming helix and the frequency of rotation, were also reduced. The effects of Zg antibodies were specific at two levels: control immunoglobulins or antibodies that bound to other flagellar surface components did not have an effect on motility, and Zg antibodies did not interfere with the motility of zoospores of oomycete species to which they did not bind. The effects of antibody-induced disruption of mastigoneme arrangement strongly support previous hypotheses that tubular mastigonemes are responsible for thrust reversal by the anterior flagellum, enabling it to pull the cell through the surrounding medium.

Keywords

Mastigonemes Monoclonal antibodies Flagellar appendages Heterokont flagellates Zoospore swimming behaviour 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen RN, Newhook FJ (1973) Chemotaxis of zoospores ofPhytophthora cinnamomi to ethanol in capillaries of soil pore dimensions. Trans Br Mycol Soc 61: 287–302Google Scholar
  2. Anderson RA, Barr DJS, Lynn DH (1991) Terminology and nomenclature of the cytoskeletal elements associated with the flagellar/cilliary apparatus in protists. Protoplasma 164: 1–8Google Scholar
  3. Bloodgood RA (1991) Transmembrane signalling in cilia and flagella. Protoplasma 164: 12–22Google Scholar
  4. Bouck GB (1971) The structure, origin, isolation and composition of the tubular mastigonemes of theOchromonas flagellum. J Cell Biol 50: 362–384Google Scholar
  5. — (1972) Architecture and assembly of mastigonemes. In: Du Praw EJ (ed) Advances in cell and molecular biology, vol 2. Academic Press, New York, pp 237–276Google Scholar
  6. —, Rosiere TK, Levasseur PJ (1990)Euglena gracilis: a model for flagellar surface assembly, with reference to other cells that bear flagellar mastigonemes and scales. In: Bloodgood RA (ed) Ciliary and flagellar membranes. Plenum, New York, pp 65–90Google Scholar
  7. Byrt PN, Grant BR (1979) Some conditions governing zoospore production in axenic cultures ofPhytophthora cinnamomi Rands. Aust J Bot 27: 103–115Google Scholar
  8. Carlile MJ (1983) Motility, taxis, and tropism inPhytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (ds)Phytophthora: its biology, taxonomy, ecology, and pathology. American Phytopathological Society, St. Paul, MN, pp 95–108Google Scholar
  9. Cavalier-Smith T (1982) The evolutionary origin and phylogeny of eukaryote flagella. In: Amos WB, Duckett JG (eds) Prokaryotic and eukaryotic flagella. Cambridge University Press, Cambridge, pp 465–494Google Scholar
  10. Cope MC, Hardham AR (1994) Synthesis and assembly of flagellar surface antigens during zoosporogenesis inPhytophthora cinnamomi. Protoplasma 180: 158–168Google Scholar
  11. Donaldson SP, Deacon JW (1993) Changes in motility ofPythium zoospores induced by calcium and calcium-modulating drugs. Mycol Res 97: 877–883Google Scholar
  12. Érsek T, Hölker U, Höfer M (1991) Non-lethal immobilisation of zoospores ofPhytophthora infestons by Li+. Mycol Res 95: 970–972Google Scholar
  13. Hardham AR, Suzaki E, Perkin JL (1986) Monoclonal antibodies to isolate-, species, and genus-specific components on the surface of zoospores of the fungusPhytophthora cinnamomi. Can J Bot 64: 311–321Google Scholar
  14. —, (1987) Microtubules and the flagellar apparatus in zoospores and cysts of the fungusPhytophthora cinnamomi. Protoplasma 137: 109–124Google Scholar
  15. —, Gubler F, Duniec J (1991) Ultrastructural and immunological studies of zoospores ofPhytophthora. In: Lucas JA, Shattock RC, Shaw DS, Cook LR (eds)Phytophthora. Cambridge University Press, Cambridge, pp 50–69Google Scholar
  16. —, Cahill DM, Cope M, Gabor BK, Gubler F, Hyde GJ (1994) Cell surface antigens ofPhytophthora spores: biological and taxonomic characterisation. Protoplasma 181: 213–232Google Scholar
  17. Heath IB, Greenwood AD, Griffiths HB (1970) The origin of flimmer inSaprolegnia, Dictyuchus, Synura andCryptomonas. J Cell Sci 7: 445–461Google Scholar
  18. Ho HH, Hickman CJ (1967) Asexual reproduction and behaviour of zoospores ofPhytophthora megasperma var.sojae. Can J Bot 45: 1963–1981Google Scholar
  19. Holwill MEJ (1982) Dynamics of eukaryotic flagellar movement. In: Amos WB, Duckett JG (eds) Prokaryotic and eukaryotic flagella. Cambridge University Press, Cambridge, pp 289–312Google Scholar
  20. —, Sleigh MA (1967) Propulsion by hispid flagella. J Exp Biol 47: 67–276Google Scholar
  21. —, Peters PD (1974) Dynamics of the hispid flagellum ofOchromonas danica. J Cell Biol 62: 322–328Google Scholar
  22. Inouye I (1993) Flagella and flagellar apparatuses of algae. In: Berner T (ed) Ultrastructure of microalgae. CRC Press, Boca Raton, pp 99–128Google Scholar
  23. Jahn TL, Landman MD, Fonsenca JR (1964) The mechanism of locomotion of flagellates. II. Function of the mastigonemes ofOchromonas., J Protozool 11: 291–296Google Scholar
  24. Markey DR, Bouck GB (1977) Mastigoneme attachment inOchromonas. J Ultrastruct Res 59: 171–177Google Scholar
  25. Nakamura S, Tanaka G, Maeda T, Kamiya R, Matsunaga T, Nikaido O (1996) Assembly and function ofChlamydomonas flagellar mastigonemes as probed with a monoclonal antibody. J Cell Sci 109: 57–62Google Scholar
  26. Sleigh MA (1964) Flagellar movement of the sessile flagellatesActinomonas, Codonosiga, Monas andPoteriodendron. Q J Microsc Sci 105: 405–414Google Scholar
  27. — (1981) Flagellar beat patterns and their possible evolution. Bio-Systems 14: 423–431Google Scholar
  28. — (1991) Mechanisms of flagellar propulsion. Protoplasma 164: 45–53Google Scholar
  29. Weste GM, Marks GC (1987) The biology ofPhytophthora cinnamomi in Australian forests. Annu Rev Phytopathol 25: 207–229Google Scholar
  30. Witman GB (1990) Introduction to cilia and flagella. In: Bloodgood RA (ed) Ciliary and flagellar membranes. Plenum, New York, pp 1–30Google Scholar
  31. Zentmyer GA (1980)Phytophthora cinnamomi and the diseases it causes. American Phytopathological Society, St. Paul, MN (Monograph 10)Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • David M. Cahill
    • 1
  • Michele Cope
    • 1
  • Adrienne R. Hardham
    • 1
  1. 1.Plant Cell Biology Group, Research School of Biological SciencesAustralian National UniversityCanberra

Personalised recommendations