Abstract
When detergent-extracted, demembranated cell models of Chlamydomonas were resuspended in reactivation solutions containing less than 10(-8) M Ca++, many models initially swam in helical paths similar to those of intact cells; others swam in circles against the surface of the slide or coverslip. With increasing time after reactivation, fewer models swam in helices and more swam in circles. This transition from helical to circular swimming was the result of a progressive inactivation of one of the axonemes; in the extreme case, one axoneme was completely inactive whereas the other beat with a normal waveform. At these low Ca++ concentrations, the inactivated axoneme was the trans-axoneme (the one farthest from the eyespot) in 70-100% of the models. At 10(-7) or 10(-6) M Ca++, cell models also proceeded from helical to circular swimming as a result of inactivation of one of the axonemes; however, under these conditions the cis-axoneme was usually the one that was inactivated. At 10(-8) M Ca++, most cells continued helical swimming, indicating that both axonemes were remaining relatively active. The progressive, Ca++-dependent inactivation of the trans- or cis-axoneme was reversed by switching the cell models to higher or lower Ca++ concentrations, respectively. A similar reversible, selective inactivation of the trans-flagellum occurred in intact cells swimming in medium containing 0.5 mM EGTA and no added Ca++. The results show that there are functional differences between the two axonemes of Chlamydomonas. The differential responses of the axonemes to submicromolar concentrations of Ca++ may form the basis for phototactic turning.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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., 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]
- Crouch T. H., Klee C. B. Positive cooperative binding of calcium to bovine brain calmodulin. Biochemistry. 1980 Aug 5;19(16):3692–3698. doi: 10.1021/bi00557a009. [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]
- 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]
- Gitelman S. E., Witman G. B. Purification of calmodulin from Chlamydomonas: calmodulin occurs in cell bodies and flagella. J Cell Biol. 1980 Dec;87(3 Pt 1):764–770. doi: 10.1083/jcb.87.3.764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodenough U. W. Motile detergent-extracted cells of Tetrahymena and Chlamydomonas. J Cell Biol. 1983 Jun;96(6):1610–1621. doi: 10.1083/jcb.96.6.1610. [DOI] [PMC free article] [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]
- Huang B., Ramanis Z., Dutcher S. K., Luck D. J. Uniflagellar mutants of Chlamydomonas: evidence for the role of basal bodies in transmission of positional information. Cell. 1982 Jul;29(3):745–753. doi: 10.1016/0092-8674(82)90436-6. [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]
- Kamiya R. Extrusion and Rotation of the central-pair microtubules in detergent-treated Chlamydomonas flagella. Prog Clin Biol Res. 1982;80:169–173. doi: 10.1002/cm.970020732. [DOI] [PubMed] [Google Scholar]
- Racey T. J., Hallett R., Nickel B. A quasi-elastic light scattering and cinematographic investigation of motile Chlamydomonas reinhardtii. Biophys J. 1981 Sep;35(3):557–571. doi: 10.1016/S0006-3495(81)84812-6. [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]
- 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]
- Smyth R. D., Berg H. C. Change in flagellar beat frequency of Chlamydomonas in response to light. Prog Clin Biol Res. 1982;80:211–215. doi: 10.1002/cm.970020740. [DOI] [PubMed] [Google Scholar]
- Stavis R. L., Hirschberg R. Phototaxis in Chlamydomonas reinhardtii. J Cell Biol. 1973 Nov;59(2 Pt 1):367–377. doi: 10.1083/jcb.59.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Witman G. B., Minervini N. Role of calmodulin in the flagellar axoneme: effect of phenothiazines on reactivated axonemes of Chlamydomonas. Prog Clin Biol Res. 1982;80:199–204. doi: 10.1002/cm.970020738. [DOI] [PubMed] [Google Scholar]
- Witman G. B., Plummer J., Sander G. Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure, composition, and function of specific axonemal components. J Cell Biol. 1978 Mar;76(3):729–747. doi: 10.1083/jcb.76.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]