Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1975 Sep 1;66(3):492–507. doi: 10.1083/jcb.66.3.492

[A functional flagella with a 6 + 0 pattern]

PMCID: PMC2109459  PMID: 169268

Abstract

The male gamete of the Gregarine Lecudina tuzetae has been studied with transmission electron microscopy and microcinematography. It is characterized by a flagellar axoneme of 6 + 0 pattern, a reduction of the chondriome, and the abundance of storage polysaccharide or lipid bodies. The movements of the flagella are of the undulating type and they are performed in the three dimensions of space. They are very slow, with a cycle time of about 2s. The structure of the axoneme components are similar to those of flagella with a 9 + 2 pattern. Each doublet has overall dimensions of 350 x 220 A; the space between the adjacent doublets is about 160 A. The A subfiber bears arms like dynein arms. The diameter of the axoneme is about 1,000 A. The basal body consists of a cylinder of dense material 2,500 A long and 1,300- 1,400 A in diameter; a microtubule 200 A in diameter is present in the axis. This study shows that a 6 + 0 pattern can generate a flagellar movement. The mechanism of the flagellar movement of the male gamete of L. tuzetae does not require the presence of central microtubules and it would include molecular interactions of the dynein-tubulin type between the adjacent peripheric doublets. The slowness of the movements is discussed in terms of the axoneme's structure and its energy supply. Finally, the phylogenetic significance of this flagella is examined on the basis of the morphopoietic potentialities of the centriolar structures.

Full Text

The Full Text of this article is available as a PDF (4.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AFZELIUS B. Electron microscopy of the sperm tail; results obtained with a new fixative. J Biophys Biochem Cytol. 1959 Mar 25;5(2):269–278. doi: 10.1083/jcb.5.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. ANDRE J. [On some newly discovered details of the ultrastructure of the vibratile organites]. J Ultrastruct Res. 1961 Mar;5:86–108. doi: 10.1016/s0022-5320(61)80007-5. [DOI] [PubMed] [Google Scholar]
  3. Aikawa M., Beaudoin R. L. Studies on nuclear division of a malarial parasite under pyrimethamine treatment. J Cell Biol. 1968 Dec;39(3):749–754. doi: 10.1083/jcb.39.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Allen R. D. A reinvestigation of cross-sections of cilia. J Cell Biol. 1968 Jun;37(3):825–831. doi: 10.1083/jcb.37.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baccetti B., Dallai R., Fratello B. The spermatozoon of arthropoda. XXII. The 12+0', 14+0' or aflagellate sperm of protura. J Cell Sci. 1973 Sep;13(2):321–335. doi: 10.1242/jcs.13.2.321. [DOI] [PubMed] [Google Scholar]
  6. Blum J. J., Lubliner J. Biophysics of flagellar motility. Annu Rev Biophys Bioeng. 1973;2:181–219. doi: 10.1146/annurev.bb.02.060173.001145. [DOI] [PubMed] [Google Scholar]
  7. Costello D. P., Henley C., Ault C. R. Microtubules in spermatozoa of childia (turbellaria, acoela) revealed by negative staining. Science. 1969 Feb 14;163(3868):678–679. doi: 10.1126/science.163.3868.678. [DOI] [PubMed] [Google Scholar]
  8. Costello D. A new theory on the mechanics of ciliary and flagellar motility. II. Theoretical considerations. Biol Bull. 1973 Oct;145(2):292–309. doi: 10.2307/1540041. [DOI] [PubMed] [Google Scholar]
  9. DAHL H. A. Fine structure of cilia in rat cerebral cortex. Z Zellforsch Mikrosk Anat. 1963;60:369–386. doi: 10.1007/BF00336612. [DOI] [PubMed] [Google Scholar]
  10. Fauré-Fremiet E. Microtubules et mécanismes morphopoïtiques. Annee Biol. 1970 Jan-Feb;9(1):1–76. [PubMed] [Google Scholar]
  11. Folliot R. Evolution des structures caudales terminales des spermatozoïdes de divers insectes Homoptères. C R Acad Sci Hebd Seances Acad Sci D. 1970 Aug 3;271(5):508–511. [PubMed] [Google Scholar]
  12. GIBBONS I. R., GRIMSTONE A. V. On flagellar structure in certain flagellates. J Biophys Biochem Cytol. 1960 Jul;7:697–716. doi: 10.1083/jcb.7.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gibbons B. H., Gibbons I. R. Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J Cell Biol. 1972 Jul;54(1):75–97. doi: 10.1083/jcb.54.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gibbons B. H., Gibbons I. R. Properties of flagellar "rigor waves" formed by abrupt removal of adenosine triphosphate from actively swimming sea urchin sperm. J Cell Biol. 1974 Dec;63(3):970–985. doi: 10.1083/jcb.63.3.970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gibbons B. H., Gibbons I. R. The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci. 1973 Sep;13(2):337–357. doi: 10.1242/jcs.13.2.337. [DOI] [PubMed] [Google Scholar]
  16. Gibbons I. R., Rowe A. J. Dynein: A Protein with Adenosine Triphosphatase Activity from Cilia. Science. 1965 Jul 23;149(3682):424–426. doi: 10.1126/science.149.3682.424. [DOI] [PubMed] [Google Scholar]
  17. Grimstone A. V., Klug A. Observations on the substructure of flagellar fibres. J Cell Sci. 1966 Sep;1(3):351–362. doi: 10.1242/jcs.1.3.351. [DOI] [PubMed] [Google Scholar]
  18. Hando T., Okada D. M., Zamboni L. Atypical cilia in human endometrium. J Cell Biol. 1968 Nov;39(2):475–481. doi: 10.1083/jcb.39.2.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Henley C., Costello D. P., Thomas M. B., Newton W. D. The "9+1" pattern of microtubules in spermatozoa of Mesostoma (Platyhelminthes, Turbellaria). Proc Natl Acad Sci U S A. 1969 Nov;64(3):849–856. doi: 10.1073/pnas.64.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jenkins R. A. Fine structure of division in ciliate protozoa. I. Micronuclear mitosis in Blepharisma. J Cell Biol. 1967 Aug;34(2):463–481. doi: 10.1083/jcb.34.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Luykx P. Cellular mechanisms of chromosome distribution. Int Rev Cytol. 1970;(Suppl):1–173. [PubMed] [Google Scholar]
  22. Phillips D. M. Exceptions to the prevailing pattern of tubules (9 + 9 + 2) in the sperm flagella of certain insect species. J Cell Biol. 1969 Jan;40(1):28–43. doi: 10.1083/jcb.40.1.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. RANDALL J., WARR J. R., HOPKINS J. M., MCVITTIE A. A SINGLE-GENE MUTATION OF CHLAMYDOMONAS REINHARDII AFFECTING MOTILITY: A GENETIC AND ELECTRON MICROSCOPE STUDY. Nature. 1964 Aug 29;203:912–914. doi: 10.1038/203912a0. [DOI] [PubMed] [Google Scholar]
  24. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. RHODIN J., DALHAMN T. Electron microscopy of the tracheal ciliated mucosa in rat. Z Zellforsch Mikrosk Anat. 1956;44(4):345–412. doi: 10.1007/BF00345847. [DOI] [PubMed] [Google Scholar]
  26. Robinow C. F., Marak J. A fiber apparatus in the nucleus of the yeast cell. J Cell Biol. 1966 Apr;29(1):129–151. doi: 10.1083/jcb.29.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ross M. M. Modified cilia in sensory organs of juvenile stages of a parasitic nematode. Science. 1967 Jun 16;156(3781):1494–1495. doi: 10.1126/science.156.3781.1494. [DOI] [PubMed] [Google Scholar]
  28. SATIR P. On the evolutionary stability of the 9 plus 2 pattern. J Cell Biol. 1962 Jan;12:181–184. doi: 10.1083/jcb.12.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. SEDAR A. W., PORTER K. R. The fine structure of cortical components of Paramecium multimicronucleatum. J Biophys Biochem Cytol. 1955 Nov 25;1(6):583–604. doi: 10.1083/jcb.1.6.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Satir P. Morphological aspects of ciliary motility. J Gen Physiol. 1967 Jul;50(6 Suppl):241–258. doi: 10.1085/jgp.50.6.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Satir P. STUDIES ON CILIA : II. Examination of the Distal Region of the Ciliary Shaft and the Role of the Filaments in Motility. J Cell Biol. 1965 Sep 1;26(3):805–834. doi: 10.1083/jcb.26.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Satir P. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J Cell Biol. 1968 Oct;39(1):77–94. doi: 10.1083/jcb.39.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sleigh M. A. Patterns of ciliary beating. Symp Soc Exp Biol. 1968;22:131–150. [PubMed] [Google Scholar]
  34. Summers K. E., Gibbons I. R. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3092–3096. doi: 10.1073/pnas.68.12.3092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Summers K. E., Gibbons I. R. Effects of trypsin digestion on flagellar structures and their relationship to motility. J Cell Biol. 1973 Sep;58(3):618–629. doi: 10.1083/jcb.58.3.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Warner F. D. New observations on flagellar fine structure. The relationship between matrix structure and the microtubule component of the axoneme. J Cell Biol. 1970 Oct;47(1):159–182. doi: 10.1083/jcb.47.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Warner F. D., Satir P. The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J Cell Biol. 1974 Oct;63(1):35–63. doi: 10.1083/jcb.63.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Warner F. D., Satir P. The substructure of ciliary microtubules. J Cell Sci. 1973 Jan;12(1):313–326. doi: 10.1242/jcs.12.1.313. [DOI] [PubMed] [Google Scholar]
  39. van Deurs B. Azonemal 12+0 pattern in the flagellum of the motile spermatozoon of Nymphon leptocheles. J Ultrastruct Res. 1973 Mar;42(5):594–598. doi: 10.1016/s0022-5320(73)80029-2. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES