Journal of Cell Science, Vol 104, Issue 1 105-117, Copyright © 1993 by Company of Biologists

JOURNAL ARTICLES

Flagellar, cellular and organismal polarity in Volvox carteri

HJ Hoops

It has previously been shown that the flagellar apparatus of the mature Volvox carteri somatic cell lacks the 180° rotational symmetry typical of most unicellular green algae. This asymmetry has been postulated to be the result of rotation of each half of the flagellar apparatus. Here it is shown that V. carteri axonemes contain polarity markers that are similar to those found in Chlamydomonas, except that in V. carteri the number one doublets do not face each other as they do in Chlamydomonas but are oriented in parallel and at approximately right angles to the line that connects the flagella. Thus, the rotational orientations of the axonemes are consistent with the postulate that the flagella of V. carteri have rotated in opposite directions, as was predicted earlier from the positions of the basal fibers and microtubular rootlets. Moreover, high-speed cinephotomicrographic analysis shows that the V. carteri flagellar effective strokes are also oriented in approximately the same direction, and in parallel planes. These results suggest that the direction of the effective stroke in both Chlamydomonas and Volvox is fixed, and that rotation of the axoneme is the cause of the differences in flagellar motility observed between Chlamydomonas and Volvox. These differences are probably essential for effective organismal motility. Cellular polarity of V. carteri can be related to that of Chlamydomonas after taking into account the developmental reorientation of flagellar apparatus components. This reorientation also results in the movement of the eyespot from a position nearer one of the flagellar bases to a position approximately equidistant between them. By analogy to Chlamydomonas, the anti side of the V. carteri somatic cell faces the spheroid anterior, the syn side faces the spheroid posterior. The cis side of the cell is to the cell's left (the right to an outside observer), although it cannot be described solely on the basis of eyespot position as it can in Chlamydomonas, while the trans side is to the cell's right. It follows that if the direction of the effective flagellar stroke is specified by structural features, then effective organismal motility in V. carteri, will be accomplished only if the cells are held in the proper orientation with respect to one another. The simplest arrangement that will yield both progression and rotation in ovoid or spherical colonies composed of biflagellate isokont cells is one in which the cells are arranged with rotational symmetry about the anterior-posterior axis of the spheroid. Analysis of the polarity of somatic cells from throughout the spheroid shows that it is constructed with just such symmetry. This symmetry probably originates with the very first divisions.
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