Abstract
The interphase flagellar apparatus of the green alga Chlorogonium elongatum resembles that of Chlamydomonas reinhardtii in the possession of microtubular rootlets and striated fibers. However, Chlorogonium, unlike Chlamydomonas, retains functional flagella during cell division. In dividing cells, the basal bodies and associated structures are no longer present at the flagellar bases, but have apparently detached and migrated towards the cell equator before the first mitosis. The transition regions remain with the flagella, which are now attached to a large apical mitochondrion by cross-striated filamentous components. Both dividing and nondividing cells of Chlorogonium propagate asymmetrical ciliary-type waveforms during forward swimming and symmetrical flagellar-type waveforms during reverse swimming. High- speed cinephotomicrographic analysis indicates that waveforms, beat frequency, and flagellar coordination are similar in both cell types. This indicates that basal bodies, striated fibers, and microtubular rootlets are not required for the initiation of flagellar beat, coordination of the two flagella, or determination of flagellar waveform. Dividing cells display a strong net negative phototaxis comparable to that of nondividing cells; hence, none of these structures are required for the transmission or processing of the signals involved in phototaxis, or for the changes in flagellar beat that lead to phototactic turning. Therefore, all of the machinery directly involved in the control of flagellar motion is contained within the axoneme and/or transition region. The timing of formation and the positioning of the newly formed basal structures in each of the daughter cells suggests that they play a significant role in cellular morphogenesis.
Full Text
The Full Text of this article is available as a PDF (6.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allen C., Borisy G. G. Structural polarity and directional growth of microtubules of Chlamydomonas flagella. J Mol Biol. 1974 Dec 5;90(2):381–402. doi: 10.1016/0022-2836(74)90381-7. [DOI] [PubMed] [Google Scholar]
- Allen R. D. Fine structure, reconstruction and possible functions of components of the cortex of Tetrahymena pyriformis. J Protozool. 1967 Nov;14(4):553–565. doi: 10.1111/j.1550-7408.1967.tb02042.x. [DOI] [PubMed] [Google Scholar]
- Atema J. Microtube theory of sensory transduction. J Theor Biol. 1973 Jan;38(1):181–190. doi: 10.1016/0022-5193(73)90233-6. [DOI] [PubMed] [Google Scholar]
- Bessen M., Fay R. B., Witman G. B. Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas. J Cell Biol. 1980 Aug;86(2):446–455. doi: 10.1083/jcb.86.2.446. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J., Luck D. J. Bending patterns of chlamydomonas flagella I. Wild-type bending patterns. Cell Motil. 1983;3(2):131–150. doi: 10.1002/cm.970030204. [DOI] [PubMed] [Google Scholar]
- Brokaw C. J., Luck D. J., Huang B. Analysis of the movement of Chlamydomonas flagella:" the function of the radial-spoke system is revealed by comparison of wild-type and mutant flagella. J Cell Biol. 1982 Mar;92(3):722–732. doi: 10.1083/jcb.92.3.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown D. L., Massalski A., Patenaude R. Organization of the flagellar apparatus and associate cytoplasmic microtubules in the quadriflagellate alga Polytomella agilis. J Cell Biol. 1976 Apr;69(1):106–125. doi: 10.1083/jcb.69.1.106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavalier-Smith T. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci. 1974 Dec;16(3):529–556. doi: 10.1242/jcs.16.3.529. [DOI] [PubMed] [Google Scholar]
- Coyne B., Rosenbaum J. L. Flagellar elongation and shortening in chlamydomonas. II. Re-utilization of flagellar proteins. J Cell Biol. 1970 Dec;47(3):777–781. doi: 10.1083/jcb.47.3.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dentler W. L. Microtubule-membrane interactions in cilia and flagella. Int Rev Cytol. 1981;72:1–47. doi: 10.1016/s0074-7696(08)61193-6. [DOI] [PubMed] [Google Scholar]
- Eckert R., Brehm P. Ionic mechanisms of excitation in Paramecium. Annu Rev Biophys Bioeng. 1979;8:353–383. doi: 10.1146/annurev.bb.08.060179.002033. [DOI] [PubMed] [Google Scholar]
- Fawcett D. W. A comparative view of sperm ultrastructure. Biol Reprod Suppl. 1970;2:90–127. [PubMed] [Google Scholar]
- Fawcett D. W., Phillips D. M. The fine structure and development of the neck region of the mammalian spermatozoon. Anat Rec. 1969 Oct;165(2):153–164. doi: 10.1002/ar.1091650204. [DOI] [PubMed] [Google Scholar]
- Foster K. W., Smyth R. D. Light Antennas in phototactic algae. Microbiol Rev. 1980 Dec;44(4):572–630. doi: 10.1128/mr.44.4.572-630.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedmann I., Colwin A. L., Colwin L. H. Fine-structural aspects of fertilization in Chlamydomonas reinhardi. J Cell Sci. 1968 Mar;3(1):115–128. doi: 10.1242/jcs.3.1.115. [DOI] [PubMed] [Google Scholar]
- Fulton C., Dingle A. D. Basal bodies, but not centrioles, in Naegleria. J Cell Biol. 1971 Dec;51(3):826–836. doi: 10.1083/jcb.51.3.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaffal K. P., Schneider G. J. Morphogenesis of the plastidome and the flagellar apparatus during the vegetative life cycle of the colourless phytoflagellate Polytoma papillatum. Cytobios. 1980;27(105):43–61. [PubMed] [Google Scholar]
- Goodenough U. W., Weiss R. L. Interrelationships between microtubules, a striated fiber, and the gametic mating structure of Chlamydomonas reinhardi. J Cell Biol. 1978 Feb;76(2):430–438. doi: 10.1083/jcb.76.2.430. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gordon M. The distal centriole in guinea pig spermiogenesis. J Ultrastruct Res. 1972 May;39(3):364–388. doi: 10.1016/s0022-5320(72)90029-9. [DOI] [PubMed] [Google Scholar]
- Gould R. R. The basal bodies of Chlamydomonas reinhardtii. Formation from probasal bodies, isolation, and partial characterization. J Cell Biol. 1975 Apr;65(1):65–74. doi: 10.1083/jcb.65.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hepler P. K. The blepharoplast of Marsilea: its de novo formation and spindle association. J Cell Sci. 1976 Jul;21(2):361–390. doi: 10.1242/jcs.21.2.361. [DOI] [PubMed] [Google Scholar]
- Hoops H. J., Witman G. B. Outer doublet heterogeneity reveals structural polarity related to beat direction in Chlamydomonas flagella. J Cell Biol. 1983 Sep;97(3):902–908. doi: 10.1083/jcb.97.3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoops H. J., Wright R. L., Jarvik J. W., Witman G. B. Flagellar waveform and rotational orientation in a Chlamydomonas mutant lacking normal striated fibers. J Cell Biol. 1984 Mar;98(3):818–824. doi: 10.1083/jcb.98.3.818. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyams J. S., Borisy G. G. Flagellar coordination in Chlamydomonas reinhardtii: isolation and reactivation of the flagellar apparatus. Science. 1975 Sep 12;189(4206):891–893. doi: 10.1126/science.1098148. [DOI] [PubMed] [Google Scholar]
- Hyams J. S., Borisy G. G. Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro. J Cell Sci. 1978 Oct;33:235–253. doi: 10.1242/jcs.33.1.235. [DOI] [PubMed] [Google Scholar]
- Johnson U. G., Porter K. R. Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules. J Cell Biol. 1968 Aug;38(2):403–425. doi: 10.1083/jcb.38.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kamiya R., Witman G. B. Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models of Chlamydomonas. J Cell Biol. 1984 Jan;98(1):97–107. doi: 10.1083/jcb.98.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kung C., Saimi Y. The physiological basis of taxes in Paramecium. Annu Rev Physiol. 1982;44:519–534. doi: 10.1146/annurev.ph.44.030182.002511. [DOI] [PubMed] [Google Scholar]
- Melkonian M., Robenek H. Eyespot membranes of Chlamydomonas reinhardii: a freeze-fracture study. J Ultrastruct Res. 1980 Jul;72(1):90–102. doi: 10.1016/s0022-5320(80)90138-0. [DOI] [PubMed] [Google Scholar]
- Melkonian M. The functional analysis of the flagellar apparatus in green algae. Symp Soc Exp Biol. 1982;35:589–606. [PubMed] [Google Scholar]
- Moestrup O. On the phylogenetic validity of the flagellar apparatus in green algae and other chlorophyll A and B containing plants. Biosystems. 1978 Apr;10(1-2):117–144. doi: 10.1016/0303-2647(78)90035-7. [DOI] [PubMed] [Google Scholar]
- Phillips D. M. Insect sperm: their structure and morphogenesis. J Cell Biol. 1970 Feb;44(2):243–277. doi: 10.1083/jcb.44.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ringo D. L. Flagellar motion and fine structure of the flagellar apparatus in Chlamydomonas. J Cell Biol. 1967 Jun;33(3):543–571. doi: 10.1083/jcb.33.3.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SAGER R., GRANICK S. Nutritional studies with Chlamydomonas reinhardi. Ann N Y Acad Sci. 1953 Oct 14;56(5):831–838. doi: 10.1111/j.1749-6632.1953.tb30261.x. [DOI] [PubMed] [Google Scholar]
- SAGER R., PALADE G. E. Structure and development of the chloroplast in Chlamydomonas. I. The normal green cell. J Biophys Biochem Cytol. 1957 May 25;3(3):463–488. doi: 10.1083/jcb.3.3.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salisbury J. L., Floyd G. L. Calcium-induced contraction of the rhizoplast of a quadriflagellate green alga. Science. 1978 Dec 1;202(4371):975–977. doi: 10.1126/science.202.4371.975. [DOI] [PubMed] [Google Scholar]
- Schmidt J. A., Eckert R. Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii. Nature. 1976 Aug 19;262(5570):713–715. doi: 10.1038/262713a0. [DOI] [PubMed] [Google Scholar]
- Stearns M. E., Brown D. L. Microtubule organizing centers (MTOCs) of the alga Polytomella exert spatial control over microtubule initiation in vivo and in vitro. J Ultrastruct Res. 1981 Dec;77(3):366–378. doi: 10.1016/s0022-5320(81)80033-0. [DOI] [PubMed] [Google Scholar]
- Stearns M. E., Connolly J. A., Brown D. L. Cytoplasmic microtubule organizing centers isolated from Polytomella agilis. Science. 1976 Jan 16;191(4223):188–191. doi: 10.1126/science.1246607. [DOI] [PubMed] [Google Scholar]
- Stephens R. E. The basal apparatus. Mass isolation from the molluscan ciliated gill epithelium and a preliminary characterization of striated rootlets. J Cell Biol. 1975 Feb;64(2):408–420. doi: 10.1083/jcb.64.2.408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- White R. B., Brown D. L. ATPase activities associated with the flagellar basal apparatus of Polytomella. J Ultrastruct Res. 1981 May;75(2):151–161. doi: 10.1016/s0022-5320(81)80131-1. [DOI] [PubMed] [Google Scholar]
- Woolley D. M., Fawcett D. W. The degeneration and disappearance of the centrioles during the development of the rat spermatozoon. Anat Rec. 1973 Oct;177(2):289–301. doi: 10.1002/ar.1091770209. [DOI] [PubMed] [Google Scholar]
- Wright R. L., Chojnacki B., Jarvik J. W. Abnormal basal-body number, location, and orientation in a striated fiber-defective mutant of Chlamydomonas reinhardtii. J Cell Biol. 1983 Jun;96(6):1697–1707. doi: 10.1083/jcb.96.6.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]