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Mitotic and Meiotic Spindles from Two Insect Orders, Lepidoptera and Diptera, Differ in Terms of Microtubule and Membrane Content

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Mitotic and Meiotic Spindles from Two Insect Orders, Lepidoptera and Diptera, Differ in Terms of Microtubule and Membrane Content Mitotic and meiotic spindles from two insect orders, Lepidoptera and Diptera, differ in terms of microtubule and membrane content KLAUS WERNER WOLF Institut ftir Biologie der Medizinischen Universit&t zu Ltibeck, Ratzburger Allee 160, D-2400 Lilbeck 1, Federal Republic of Germany Summary Spindles from the gonads of five insect species were tors of 1.8 to 3.0. The correlation between the amount examined after conventional preparation for elec- of spindle membranes and the microtubule content tron microscopy. The aim of the study was to deter- of the spindle indicates a functional relationship. mine (1) the range of variation of the spindle mem- Spindle membranes are believed to influence micro- branes between mitotic and meiotic cells and (2) the tubule stability via the regulation of the Ca2+ concen- correlation of possible differences with the micro- tration within the spindle area. The high microtubule tubule content of the spindles. The study involved mass in spindles from Lepidoptera spermatocytes four moth species, Ephestia kuehniella, Phragmato- may result from the membrane-dependent lowering bia fuliginosa, Orgyia thyellina, Orgyia antiqua, and of the Ca2+ level within the spindles. Finally, an one fly, Megaselia scalaris. Somatic and gonial unconventional idea on the role of intraspindle mem- mitoses in all species examined showed a sparse branes is offered. This concept is not intended to spindle membrane inventory. In contrast, spermato- challenge the function of spindle-associated mem- cytes consistently had a multi- layered spindle envel- branes as Ca2+-sequestrating compartments. Intras- ope. In spermatocytes of all Lepidoptera species pindle membranes are considered as stuffing examined, but not in those of M. scalaris, diverse material in sheathed spindles. Membranous com- forms of intraspindle membranes existed in addition partments reduce the free volume within the spindle. to the spindle envelope. Microtubule counts in Thereby, monomeric tubulin is concentrated and the serially cross-sectioned spindles of E. kuehniella re- formation of microtubules is favoured. vealed an about 6-fold increase in the mass of polym- erized tubulin during the transition from spermato- gonia to primary spermatocytes. The increase was 3.3-fold in O. thyellina and less than 3-fold in M. sca- Key words: mitosis, meiosis, Ephestia kuehniella, Orgyia laris. The density of intraspindle membranes in antiqua, Orgyia thyellina, Phragmatobia fuliginosa, Megaselia E. kuehniella was higher than in O. thyelhna by fac- scalaris. Introduction The function of spindles is to supply the daughter cells with a euploid set of chromosomes. In mitotic anaphase, The dominant component of spindles is the microtubular chromatids migrate towards the spindle poles, whereas in cytoskeleton. Microtubules (MTs) most probably play a anaphase I half-bivalents segregate. The total mass of role in chromosome migration (for reviews, see Nicklas, migrating material does not differ between mitosis and 1988; Mclntosh, 1989; Mitchison, 1988). During the last meiosis I. On this premise, prominent structural differ- decade, membranous components moved from the fringes ences between mitotic and meiotic spindles are not readily to the focus of studies aimed at spindle structure and anticipated. However, the comparison of spindles in sper- function (for reviews, see Paweletz, 1981; Hepler and matogonia and spermatocytes of the Hemiptera species Wolniak, 1984; Hepler, 1989a). Alhough, as yet, a satisfy- Dysdercus intermedius (Motzko and Ruthmann, 1984) ing conceptual framework has not been derived from the revealed striking differences in the membrane inventory. available data, spindle membranes seem to be involved in Therefore it seemed worthwhile to concentrate on the Ca2+ transients and spindle dynamics (for detailed dis- issue of spindle dimorphism in higher eukaryotes. cussions, see Wolniak, 1988; Hepler, 19896). Three types of In the present study, dividing mitotic cells and sper- membrane systems linked with spindles can be dis- matocytes from five insect species are compared, with a tinguished. (1) Intraspindle membranes occur together focus on two key components: membranes associated with with microtubules (MTs) and chromosomes within the the spindle and the microtubular cytoskeleton. Four Lepi- spindle domain. They are often arranged parallel to the doptera species, Orgyia thyellina (n=ll; Cretschmar, kinetochore MTs. (2) Perispindle membranes surround the 1928), Orgyia antiqua (n=14; Cretschmar, 1928), Ephestia spindle apparatus. (3) Astral membranes or lamellae are kuehniella (n=30, Traut and Mosbacher, 1968) and Phrag- arranged parallel to MTs radiating out from the spindle matobia fuliginosa, have been examined. The karyotype of poles. the latter species contains a giant sex chromosome pair. Journal of Cell Science 97, 91-100 (1990) Printed in Great Britain © The Company of Biologists Limited 1990 91 Chromosome races with haploid numbers of 28 and 29 Results chromosomes are known in this species (Seiler, 1925). The individuals used in the present study have a haploid Lepidoptera chromosome number of 29. Observations on the phorid fly Somatic mitosis in cells of the testicular sheath (Fig. 1) Megaselia scalaris are also presented. In addition to the and of the imaginal disks in E. kuehniella is characterized regular three chromosome pairs (see Johnson et al. 1988, by a sparsely developed spindle envelope. One, and in and references therein), the karyotype of this species places two, discontinuous layers of membranous sheets contains varying numbers of centromere-like elements surround the spindle domain. The two membrane layers without chromosome arms (Wolfed al. 1988). are not closely associated and spindle MTs are found The spindle membrane inventory and the MT mass were between them. Intraspindle membranes are very scarce found to differ between mitotic cells and spermatocytes in and form flat or spherical vesicles (Fig. 1, inset). A pair of all species examined. orthogonally arranged centrioles is connected with each spindle pole. This also applies to spindle poles in all other mitotic cells examined in this study. The centrioles are embedded in pericentriolar material of moderate density. Metaphase spindles in imaginal disks of O. antiqua are Materials and methods identical to those in E. kuehniella regarding spindle mem- branes. Somatic mitosis in 0. thyellina and P. fuliginosa Laboratory strains of the Mediterranean mealmoth, E. kuehniella was not studied. (Pyralidae), were raised on rolled oats. One strain, L, has a haploid chromosome number of 30. A second strain used, W10, Spermatogonia of E. kuehniella have a one- to three- contains a small heterochromatic fragment in addition to the 30 layered fenestrated spindle envelope. Large gaps occur in chromosomes. This fragment is derived from the W-chromosome the vicinity of the basal bodies (Fig. 2). The individual (Traut et al. 1986). Spindle morphology does not vary between the membranous cisternae forming the spindle envelope have two strains and for the present purpose no distinction is made little space between one another. Intraspindle membranes between them. Testes and imaginal disks of the wings from larvae in the last instar were prepared for electron microscopy according are missing. Metaphase and early anaphase spindles in to Wolf (1987). gonial cells of 0. thyellina (Fig. 3), 0. antiqua (Fig. 4), and P. fuliginosa (not shown), closely resemble those in sper- The same protocol was followed for gonads and imaginal disks of the wings from last instar larvae of O. thyellina and 0. antiqua matogonia of E. kuehniella. (Lymantriidae). Larvae of these two species were kindly provided Lepidoptera produce two types of sperm (for reviews, see by Sir C. Clarke (Liverpool, UK). In addition, eggs of O. antiqua Fain-Maurel, 1966; Silberglied et al. 1984). Eupyrene were collected in Sandhausen (FRG). The larvae from this isolate spermatocytes (for terminology, see Meves, 1903) give rise hatched in the laboratory and were fed with bramble leaves. to fertile spermatozoa. Apyrene spermatocytes develop Larvae of P. fuliginosa (Arctiidae) were collected in Bergedorf into sterile sperms. The two types of spermatocytes can be near Hamburg (FRG) and raised on leaves of Plantago. Testes readily distinguished from one another. Eupyrene sper- from last instar larvae of the third and fourth laboratory gener- ation were processed for electron microscopy as described pre- matocytes are generally larger, possess a normal spindle, viously (Wolf, 1987). and form a metaphase plate. In contrast, in apyrene Two laboratory strains of M. scalaris (Phoridae), referred to as spermatocytes diverse deviations from regular develop- Wien' and Tennessee' (Johnson et al. 1988), were examined. ment occur (see Wolf et al. 1987). This study deals exclus- Differences in spindle structure are not apparent and the two ively with eupyrene meiosis. strains are not treated separately in the present study. The larvae As a rule, spindles in spermatocytes have a larger pole- were grown on a modified Drosophila medium (Johnson et al. to-pole distance and a larger volume than mitotic spindles. 1988). Pupae were dissected in an isotonic saline (Hayes, 1953). Differences in cell size and the presence of one or two basal Subsequently the gonads were transferred into lml saline sol- ution containing 2.5% glutaraldehyde. After 5min, 3 ml of 8% bodies per spindle pole distinguish secondary and primary tannic acid in phosphate buffer (67 nw, pH 6.8) were
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