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Unorthodox Male Meiosis in Trichosia Pubescens

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Unorthodox Male Meiosis in Trichosia Pubescens Journal of Cell Science 107, 299-312 (1994) 299 Printed in Great Britain © The Company of Biologists Limited 1994 JCS8407 Unorthodox male meiosis in Trichosia pubescens (Sciaridae) Chromosome elimination involves polar organelle degeneration and monocentric spindles in first and second division Harald Fuge Department of Biology, University of Kaiserslautern, PO Box 3049, D-67653 Kaiserslautern, Federal Republic of Germany SUMMARY Male meiosis in Trichosia pubescens (Sciaridae) was inves- moves towards the pole, paternal chromosomes seem to be tigated by means of serial section electron microscopy and unable to contact the pole, possibly due to an inactivation immunofluorescence light microscopy. From earlier studies of their kinetochores. Retrograde (‘away from the pole’) of another sciarid fly, Sciara coprophila (Phillips (1967) J. chromosome motion not involving kinetochores is assumed. Cell. Biol. 33, 73-92), it is known that the spindle poles in Eventually, paternal chromosomes move into the pole- sciarid spermatogonia are characterized by pairs of ‘giant distal bud and are eliminated by casting off, together with centrioles’, ring-shaped organelles composed of large the components of the degenerate polar organelle. Chro- numbers of singlet microtubules. In the present study sper- mosome elimination can be delayed until the second matocytes in early prophase of Trichosia were found to meiotic division. The spindle of the second meiotic division possess single giant centrioles at opposite sides of the is bipolar and monocentric. One spindle pole is marked by nucleus. The obvious reduction in centriole number from the polar centre of first division. The opposite spindle apex the spermatogonial to the spermatocyte stage is suggested is devoid of a polar centre. It is assumed that spindle bipo- to be the result of a suppression of daughter centriole larity in the second division is induced by the amphi-ori- formation. In late prophase, a large aster is developed entated chromosomes themselves. The maternal and L around the centriole at one pole. At the opposite pole no chromosome set (except the non-disjunctional X chromo- comparable aster is formed. Instead, a number of irregular some, which is found near the polar centre) congress in a centriolar components appear in this region, a process that metaphase plate, divide and segregate. Of the two daughter is understood to be a degeneration of the polar organelle. nuclei resulting from the second meiotic division, the one The components of the degenerate pole migrate into a cyto- containing the X chromatids is retained as the nucleus of plasmic protrusion (‘bud’), which later is also utilized for the future spermatozoon. The other nucleus becomes again the elimination of paternal chromosomes. The existence of eliminated within a second cytoplasmic bud. only one functional polar centre is the reason for the formation of a monopolar monocentric spindle in first meiotic division, which in turn is one of the prerequisites Key words: giant centriole, spindle formation, kinetochore for the elimination of paternal chromosomes. While the set orientation, monopolar monocentric division, bipolar monocentric of maternal and L chromosomes orientates and probably division, serial section electron microscopy, immunofluorescence INTRODUCTION In the following, a synopsis of only those events that were the subject of the present investigation is given. The spermatocyte Since Metz’ pioneering work (Metz, 1927, 1931, 1933; Metz enters the first meiotic division with a diploid set of univalent, et al., 1926) male meiosis of sciarid flies has been repeatedly i.e. unpaired chromosomes consisting of ordinary autosomes, investigated (e.g. see Rieffel and Crouse, 1966; Phillips, 1966, germline limited chromosomes (L chromosomes), and two X 1967; Amabis et al., 1979; Abbott and Gerbi, 1981; Abbott et chromosomes. The first meiotic division is characterized by the al., 1981; Kubai, 1982, 1987). It is especially interesting with formation of a monopolar spindle. Chromosomes inherited respect to unusual orientation and movement of chromosomes from the mother (maternal chromosomes) together with L during non-random segregation and elimination in the first chromosomes and those inherited from the father (paternal meiotic division. A comprehensive review was presented by chromosomes) are non-randomly distributed. Maternal chro- Gerbi (1986). Apart from Amabis et al. (1979), who investi- mosomes (autosomes and one X chromosome) and L chromo- gated meiosis in Trichosia pubescens using standard light somes are displaced to the pole of the monopolar spindle, microscopical techniques, most other workers studied whereas paternal chromosomes (autosomes and one X chro- members of the genus Sciara, particularly Sciara coprophila. mosome) become eliminated in a cytoplasmic protrusion 300 H. Fuge (‘bud’). With respect to autosomes and the X this directed seg- matocytes. The suspended spermatocytes were slightly separated with regation is reductional. Kinetochores of paternal chromosomes a fine needle, an 18 mm × 18 mm coverslip was applied, and fixation of Sciara were found to be connected with the pole via kine- was carried out under the coverslip. tochore microtubules (Kubai, 1982), although the chromo- Electron microscopy somes become eliminated. Whether or not the paternal haploid set is definitely ‘backing away’ from the spindle pole is a The first fixation was carried out for 30 minutes at room temperature in 0.03 M Pipes buffer (pH 7) containing 2% glutaraldehyde. After matter of controversy (Gerbi, 1986). The second meiotic fixation the coverslip was removed by dipping the slide in buffer. The division in male sciarids is bipolar (Gerbi, 1986). Maternal selection of appropriate cell stages in the embedded material with the autosomes and L chromosomes congress in a metaphase plate phase-contrast microscope is prevented by a dense layer of mito- and their chromatids are conventionally distributed to opposite chondria masking the nuclei and division spindles of Trichosia sper- poles in anaphase (equational division). The maternal X chro- matocytes. For this reason, chromosomes were stained with DAPI mosome does not divide but is found at one pole already at (4′,6-diamidino-2-phenylindole-dihydrochloride, 2×10−5% in a 1:1, metaphase (‘precocious’ X chromosome; Abbott and Gerbi, glycerol/phosphate-buffered saline (PBS) medium) prior to second 1981). Two daughter nuclei are formed and, while the nucleus fixation and resin embedding, and examined with the fluorescence containing both chromatids of the X is retained as the future microscope. The positions of appropriate stages were recorded and spermatid nucleus, the other nucleus is again eliminated in a the chromosomes photographed. Then the cells were washed in buffer, fixed for 30 minutes in 0.03 M Pipes containing 1% OsO4, cytoplasmic bud. Hence, male meiosis results in a single sper- dehydrated in an acetone series, and flat-embedded on the slide in a matozoon containing only chromosomes inherited from the drop of Vestopal W polyester resin. After removal from the slide the mother and the L chromosomes. According to Amabis et al. selected cells (prophase stages, 9 cells from 7 animals; first meiotic (1979) male meiosis in Trichosia pubescens is similar to that division, 8 cells from 4 animals; interkinesis, one cell; second meiotic in Sciara, with the exception that paternal chromosomes division including telophase stages, 15 cells from 7 animals) were obviously are not orientated polewards during the first meiotic sectioned with a LKB Ultrotome III (section thickness 50 nm). division. In a preliminary study using indirect immunofluor- Sections were double-stained with uranyl acetate and lead citrate, and escence staining of tubulin Bastmeyer (1989) observed that one examined with a Zeiss EM10A electron microsocope working at 80 spindle pole in the second meiotic division in Trichosia lacked kV. aster microtubules. Immunofluorescence In conclusion, male sciarid meiosis does not seem to be less The cells were fixed in 0.03 M Pipes (pH 7) containing 2.5% enigmatic today than it was in the time of Metz. Regarding the formaldehyde (freshly prepared from paraformaldehyde), 0.5% glu- general problem of spindle function in mitosis and meiosis the taraldehyde, 0.2% Triton X-100, 1 mM EGTA, and 1 mM MgCl2 for study of such ‘exceptional’ cases is a meaningful attempt, to 10 minutes. After fixation slides were washed 3 times for 5 minutes cite a statement of the late Max Hartmann: ‘...Ihre (der Sciari- in PBS (pH 7), or stored for longer at 4°C in the same buffer. Tubulin denmeiose) Analyse könnte deshalb für das Mitoseproblem staining: cells were incubated with anti-α-tubulin (mouse monoclonal aufschlußreicher sein, als wiederholte Untersuchungen an der antibody, IgG1, Serva, Heidelberg, 1:2000 dilution in PBS) for 1 hour ‘normalen’ Mitose. Ehe es nicht gelingt, alle verschiedenen at room temperature. Three 5-minute rinses in PBS were followed by Mitoseabläufe einer einheitlichen Vorstellung einzuordnen, incubation in fluorescein isothiocyanate (FITC)-conjugated anti- kann das Rätsel vom Mechanismus der Kernteilung nicht als mouse IgG (affinity-isolated antibody, Sigma Chemical Co., St Louis; 1:100 dilution in PBS) for 30 minutes at room temperature. After gelöst angesehen werden.’ (Hartmann, 1953). rinsing three times for 5 minutes in PBS (with the last step contain- The data of the present study of spermatogenesis in ing 2×10−5% DAPI for chromosome staining) the slides were Trichosia are based
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