Studies of Spermatogenesis in the Hepaticae V. Blepharoplast Development in Marchantia polymorpha

Abstract

Coaxial centrioles and a microtubule organizing center (MTOC) constitute each centrosome in spermatid mother cells of Marchantia polymorpha. During cell division the centrosome separates at its midregion and the two centrioles undergo a planar rotation that brings them to lie somewhat staggered and nearly parallel with their proximal ends embedded in osmiophilic granular material similar in appearance to that of the MTOC. Microtubules of the multilayered structure (MLS) arise in this material below the posterior centriole and parallel to its long axis. The rotation of centrioles and the initiation of S1 tubules below the posterior centriole determine polarity of the incipient blepharoplast. Lower MLS strata are formed under the anterior centriole by the compaction of granular, osmiophilic matrix. Formation and growth of S2 vertical lamellae occur at the left front edge of the MLS in association with MTOC‐like matrix localized near the cell membrane. The MLS enlarges to about 0.4 μm wide by 0.6 μm long and is ovoid in outline except for a short distal projection underlying the posterior centriole. Subsequently the lamellae are transformed into homogenous, osmiophilic matrix that contributes directly to the expansion of all MLS strata including microtubules. The stratum of lamellae is interpreted as a planar MTOC subject to morphogenetic control. Each of the four strata grows proximally while the tapering distal projection lengthens beneath the posterior basal body. Dense matrix above the MLS, apparently elaborated by the S2 layer, is organized into cartwheel and triplet components of the basal bodies’ proximal extensions. Organization of triplet tubules proceeds from proximal to distal toward preexisting triplets. Osmiophilic matrix contributes to the formation of microtubule keels and osmiophilic crests and may serve as a cementing material that stabilizes the spatial relationships of blepharoplast components. After full expansion of the MLS’ lower strata, the S2 layer is reorganized into lamellae. Flagellar growth in Marchantia is postulated to involve a process whereby subunits or their precursors are elaborated by the MLS, translocated to the distal end of the flagellum and incorporated into the axonemal tubules. When MLS microtubules elongate to form a long, narrow band, the distal half of the S2 layer is again in the osmiophilic matrix state.

Ultrastructural studies of mutant spermatozoids in ferns. I. The mature nonmotile spermatozoid of mutation 230X in Ceratopteris thalictroides(L.)Brongn

“…They are almost identical in appearance to those of the mid-spermatids of both the wild type and 230X [Duckett, Klekowski and Hickok, unpublished data]. It has now been well documented in both bryophytes and pteridophytes, that changes in the substructure of the MLS lamellar strip are closely correlated with the rate of growth of the microtubular band and axonemes at particular stages in gamete metamorphosis Duckett, 1973;Duckett and Bell, 1977;Kreitner and Carothers, 1976;Moser et al, 1977;Robbins and Carothers, 19781. It may well be that the apparently immature condition of the lamellae in the mature gametes of 230X is related to the fact that some of the tubulin normally destined for the MLS is polymerized elsewhere as abnormal flagella.…”

“…Antithetically, colchicine produces irregularities in both the cytoskeletal (MLS) and axonemal tubules in Nitella [Turner, 19701 ,Marsilea [Myles and Hepler, 1977a,b], and Ceratopteris [Duckett, unpublished data]. However, it should be noted that Wilkinson et al [1975] were able to distinguish between these two classes of tubules in D m sophila spermatids on the basis of vinblastine treatmentall but the cross-linked manchette tubules were absent in the presence o f the drug, phytes [Carothers, 1973[Carothers, , 1975Kreitner, 1977a,b;Kreitner and Carothers, 1976;Moser et al, 19771 and pteridophytes [Carothers et al, 1975;Duckett, 1973Duckett, ,1975Duckett and Bell, 1977;Myles and Hepler, 1977a,b] , there is general agreement that the lamellar strip constitutes an elaborate microtubule-organizing center responsible for the coordinated assembly of the overlying microtubular band. The only ordered arrays of regularly spaced microtubules in 230X are those in contact with the MLS lamellar strip; and this is strong supporting evidence for this hypothesis.…”

“…The striking series of correlations between abnormal nuclear shapes and aberrant microtubule arrays described in this paper in mutation 230X of Ceratopteris, furnishes the means for discriminating between these contrasting ideas. Finally, this mutation provides a system for examining the widely held, but as yet completely unproven view, that the anterior lamellar portion of the multilayered structure (the lamellar strip [Duckett, 19731 ) acts as the initiating site (microtubule In the vast majority of mutations that affect flagellar motility, ultrastructural studies organizing center), which effects the coordinated synthesis of the regularly spaced tubules of the microtubular band [Carothers and Duckett, 1978;Duckett, 1975;Kreitner and Carothers, 1976;Myles and Hepler, 1977al.…”

Ultrastructural Studies of Spermatogenesis in the Anthocerotales. I. The Blepharoplast and Anterior Mitochondrion in Phaeoceros Laevis: Early Development

“…24). Kreitner and Carothers (1976) interpret the MLS, centrioles and their derivative basal bodies, together with the granular matrix associated with them as a highly structured microtubule organizing center (MTOC) (Pickett-Heaps, 1971). The present data on Phaeoceros lends strong support to this contention.…”

“…In very young spermatids the nascent MLS appears immediately below the centrioles with the anterior ends of the S, tubules and the proximal ends of the centrioles embedded in the same granular matrix. Throughout the subsequent periods of extensive microtubule elaboration in spermatids of both Phaeoceros and Marchantia (Kreitner and Carothers, 1976) this material is always conspicuous, and in many instances it is impossible to discriminate between the matrix and the walls of the tubules. Furthermore, short lengths of single microtubules are commonly found in association with the granular matrix around young centrioles.…”