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Basal Bodies and Associated Structures Are Not Required for Normal Flagellar Motion Or Phototaxis in the Green Alga Chlorogonium Elongatum

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Basal Bodies and Associated Structures Are Not Required for Normal Flagellar Motion Or Phototaxis in the Green Alga Chlorogonium Elongatum SUNY Geneseo KnightScholar Biology Faculty/Staff Works Department of Biology 1985 Basal bodies and associated structures are not required for normal flagellar motion or phototaxis in the green alga Chlorogonium elongatum Harold J. Hoops SUNY Geneseo George B. Witman Follow this and additional works at: https://knightscholar.geneseo.edu/biology This work is licensed under a Creative Commons Attribution-Noncommercial 3.0 License Recommended Citation Hoops H.J., Witman G.B. (1985) Basal bodies and associated structures are not required for normal flagellar motion or phototaxis in the green alga Chlorogonium elongatum. Journal of Cell Biology 100: 297-309. doi: 10.1083/jcb.100.1.297 This Article is brought to you for free and open access by the Department of Biology at KnightScholar. It has been accepted for inclusion in Biology Faculty/Staff Works by an authorized administrator of KnightScholar. For more information, please contact [email protected]. Published Online: 1 January, 1985 | Supp Info: http://doi.org/10.1083/jcb.100.1.297 Downloaded from jcb.rupress.org on August 22, 2019 Basal Bodies and Associated Structures Are Not Required for Normal Flagellar Motion or Phototaxis in the Green Alga Chlorogoniumelongatum HAROLD J. HOOPS and GEORGE B. WlTMAN Cell Biology Group, Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts01545 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. A large body of evidence has implicated the basal body as a To determine unequivocally whether the basal bodies have necessary precursor to flagellum formation, even in cases any role in flagellar movement, it would be ideal to compare where no basal bodies or centrioles exist in nonflagellated the repertoire of flagellar behavior in an intact cell in the stages of the life cycle (11, 24, 31, 48, 51). The basal bodies presence and absence of basal bodies. A recent report that the and their associated rootlets and fibers have also been pro- basal bodies separate from the flagella yet the flagella remain posed to play various roles in the functioning of individual functional in dividing cells of Polytoma (25, 26) suggested to flagella and in the coordination between flagella of the same us that such a comparison may be possible in certain members cell (10, 34, 39, 58, 59, 68), although there has been little of the Chlorophyceae. We report here that a similar situation experimental evidence in support of these roles. Clearly, the occurs in the biflagellate green alga Chlorogonium. Prior to basal body is not required for flagellar movement per se, division, the basal bodies detach from the parental flagella, because the flagella of certain mammalian and insect sperm which remain motile in the absence of associated basal bodies, are motile in the absence of basal bodies (16, 17, 28, 49, 50, microtubular rootlets, and striated fibers. We have examined 69). Moreover, isolated, demembranated flagella lacking basal flagellar waveform and beat frequency in interphase and bodies can be reactivated (1, 5); these reactivated flagella beat dividing cells of Chlorogonium and find that there is virtually with normal waveforms and even change their waveforms in no difference in the behavior of the flagella in the two cell response to Ca ÷÷ (5), the normal physiological effector (60). types. Moreover, both interphase and dividing cells swim in The JOURNAL OF CELL BIOLOGY • VOLUME 100 JANUARY 1985 297-309 © The Rockefeller University Press . 0021-9525/85/01/0297/13 $1.00 297 helices, undergo the photophobic response, and exhibit strong resuspended in modified Chlamydomonas medium 1. Cell suspensions were negative phototaxis. These results indicate that, at least in placed in chambers similar to those used for filming free swimming cells, except that the chamber depth was increased to 0.15 to 0.20 mm. Ceils were observed Chlorogonium, the basal bodies, striated fibers, and microtu- with a dim beam passed through a deep red filter (Coming # 2404, Coming bular rootlets are not required for, and probably have no role Glass Works, Corning, NY) placed over the field diaphragm. The stimulating in, the initiation or control of flagellar movement, or in the beam was provided by an American Optical Universal Focusable Illuminator signal transduction and processing required for the photopho- (American Optical Corp. Instrument Division, P.O. Box 123, Buffalo, NY) operated at the highest intensity. The beam was focused on the slide at a 10" bic response or phototaxis. All elements directly involved in angle from horizontal; the distance between the illuminator and slide was 15 the control of flageUar movement must therefore be located cm. Cells were allowed to reorient to the light for 60-75 s and then scored as in the flagellar shaft distal to the basal body. swimming towards or away from the illuminator as their images passed over a linear ocular micrometer scale oriented perpendicular to the direction of the MATERIALS AND METHODS stimulating beam. Scoring was stopped after 100 ceils had been scored or when only a few cells remained swimming through the center portion of the chamber. Each slide was treated as a separate experiment; data from slides in which <30 Cells and Culture Conditions: Chlorogoniumelongatum Dang. cells were scored were excluded from the analysis. In the control experiments (culture #11) was obtained from the Culture Collection of Algae at the Univer- the stimulating illuminator was turned off. sity of Texas at Austin (62). Unless otherwise stated, cells were grown in 125 ml of Chlorogonium growth medium composed of 80% Chlamydomonas Analysis of Eyespot Position: To determine the eyespot position of medium ! (56) modified to contain three times the normal amount of phosphate swimming cells, mixed populations of dividing and nondividing cells were buffer and 20% Euglena medium (62) in unaerated 250 ml Erlenmeyer flasks prepared as for the analysis of swimming speed and paths. Cell tracks were at 25°C under a 16:8 h light:dark cycle. Partial synchrony in cell division was filmed by darkfield illumination on Tri-X 35-mm film and developed at ASA obtained by inoculating -7 ml of a stationary culture into 125 ml fresh medium 1600 with Perfection XR-I developer (Perfection Photographic Products, Inc., -2 h before the onset of the dark period. 15 h later a mixed population Los Angeles, CA). Dilute suspensions of cells were strobed at 4-10 Hz while containing -15-20% dividing cells was obtained. For some experiments, cells the shutter was held open for 1-4 s. Eyespots were visible as bright refractile were grown in 100% Chlamydomonas medium I (modified as above) contin- spots inside the dimmer track produced by the cell body (37). uously bubbled with a 5% CO2-95% air mixture at 24"C. Under these conditions To determine which of the daughter cells retained the parental eyespot, ~ 10% of the cells were dividing during the last 2 h of the dark period, when populations of cells were grown in modified Chlamydomonas medium 1 and they were tested for phototaxis. prepared as for the waveform analysis, but viewed under darkfield illumination. Cells were scored as having two, four, or eight daughter cells, and the eyespot Electron Microscopy: Preparation for electron microscopy was as was scored as being in the daughter cell with the parental flagella or in another described previously (32), except that the initial glutaraldehyde fixation was cell. Cells in which the eyespot could not be unambiguously identified, and carried out in Chlorogoniumgrowth medium. those without motile flagella, were not scored. Analysis of Flagellar Waveform: For study of flagellar waveform, 15 ml of a cell culture containing both dividing and nondividing cells was RESULTS centrifuged in a 15-ml conical polystyrene tube at 150 g for 3 min in a clinical centrifuge at room temperature and the excess medium removed by aspiration. Life Cycle of Chlorogonium The pellet was resuspended in -0.3 ml of the remaining medium. A small aliquot of this cell suspension was placed on a clean slide and covered with a Chlorogonium elongatum is a biflagellate green alga closely coverslip. The size of this aliquot was varied until a few ceils were gently related to Chlamydomonas (6, 23). In our culture, cells are trapped between the slide and coverslip. Almost all dividing and nondividing spindle-shaped, 10 to 25 #m long, and possess a massive cells retained motile flagella throughout these procedures.
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