Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-24T18:56:54.977Z Has data issue: false hasContentIssue false

Virus-like particles, bacteria and microsporidia affect spindle-associated membranes in spermatocytes of Lepidoptera species

Published online by Cambridge University Press:  26 September 2008

Klaus Werner Wolf
Affiliation:
Institut für Anthropologie, Johannes Gutenberg-Universität Mainz, Colonel Kleinmann Weg 2a, D-55128 Mainz, Germany.

Summary

Larval testes of four Lepidoptera species were examined using electron microscopy. The testes of one species, the Mediterranean mealmoth Ephestia kuehniella (Pyralidae), were devoid of intracellular pathogens and serve as a control. In this species, metaphase spindles of primary spermatocytes showed a thick layer of perispindle membranes. The membranes were structurally very similar to the agranular endoplasmic reticulum. Membranes of this type occurred also at high frequency throughout the spindle matrix. The analysis of larval testes of Pieris brassicae (Pieridae) revealed virus-like particles within spermatocytes. In another species, Philudoria potatoria (Lasiocampidae), the spermatocytes possessed intracellular bacteria. Whereas the pathogens were found within the germ cells in these species, a fourth species, Plutella xylosteUa (Plutellide), showed microsporidia within somatic cells of the testis sheath. In all the infected animals, the mass of perispindle membranes was reduced in comparison with spermatocytes of E. kuehniella. However, spindle structure appeared regular in the infected animals. This indicates that a thick layer of perispindle membranes is not decisive for spindle assembly and function in male meiosis of Lepidopera

Type
Article
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afzelius, B.A., Alberti, G., Dallai, R., Godula, J. & Witalinski, W. (1989). Virus- and rickettsia-infected sperm cells in arthropods. J. Invertebr. Pathol. 53,375–77.CrossRefGoogle Scholar
Avery, S.W. & Anthony, D.W. (1983). Ultrastructural study of early development of Nosema algerae in Anophelesalbimanus.J. Invertebr. Pathol. 42, 8795.CrossRefGoogle Scholar
Brooks, W.M., Hauard, E.I. & Becnel, J. (1985). Two new species of Nosema (Microsporidia: Nosematidae) from the Mexican bean beetle Epilachna varivestis (Coleoptera:Coccinnelidae). J. Protozool. 32,525–35.CrossRefGoogle Scholar
Callaini, G., Giovanna, M. & Dallai, R. (1994). The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. J. Cell Sci. 107, 673–82.CrossRefGoogle ScholarPubMed
Canning, E.U. (1988).Nuclear division and chromosome cycle in microsporidia. BioSystems 21, 333–40.CrossRefGoogle ScholarPubMed
Degruguillier, M.E. (1989).Virus-like particles in testes of Heliothis virescens, Heliothis subflexa, and backcross males derived from the hybridization of Heliothis virescens males × Heliothis subflexa females. J. Invertebr. Pathol. 54, 281–99.CrossRefGoogle Scholar
Degruguillier, M.E. & Newman, S.M. Jr (1993). Hereditary viruses of Heliothis? Chromatin-associated virus-like particles in testes of six species of Heliothis and Helicoverpa, F1, and backcross males. J. Invertebr. Pathol. 61, 147–55.CrossRefGoogle Scholar
Ding, R., McDonald, K. L. & Mclntosh, J.R. (1993). Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120, 141–51.CrossRefGoogle ScholarPubMed
Friedländer, M. & Reynolds, S.E. (1988). Meiotic metaphases are induced by 20-hydroxyecdysone during spermatogenesis of the tobacco hornworm, Manduca sexta. J. Insect Physiol. 34, 1013–19.CrossRefGoogle Scholar
Friedlander, M. & Wahrman, J. (1970). The spindle as a basal body distributor: a study in the meiosis of the male silkworm moth, Bombyx mori. J. Cell Sci. 7, 6589.CrossRefGoogle ScholarPubMed
Heath, I.B. (1980). Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis? Int. Rev. Cytol. 64, 180.CrossRefGoogle ScholarPubMed
Hepler, P.K. (1989). Calcium transients during mitosis: observations in flux. J. Cell Biol. 109, 2567–73.CrossRefGoogle ScholarPubMed
Holm, P.B. & Rasmussen, S.W. (1980). Chromosome pairing recombination nodules and chiasma formation in diploid Bombyx males. Carlsberg Res. Commun. 45, 483548.CrossRefGoogle Scholar
Lai-Fook, J. (1982). Structural comparison between eupyrene and apyrene spermiogenesis in Cal podea ethlius (Hesperiidae, Lepidoptera). Can. J. Zool. 60, 1216–30.CrossRefGoogle Scholar
Leclerq-Smekens, M. (1978). Reproduction d'Euproctis chrysorrhea L. (Lépidoptère Lymantriidae) I. Etude de l'organogénèse des testicules et de la spermatogénse. Acad. R. Belg., Sec. 564, 304–17.Google Scholar
Meves, F. (1903). Ueber oligopyrene and apycene Spermien und ¨ber ihre Entstehung nach Beobachtungen an Paludma und Pygaera. Arch. Mikrosk. Anat. Ent wickl ungsges. 61, 184.Google Scholar
Moutairou, K.Schwab-Stey, H.Wemer, K.Werner, M. (1993). Microsporidia in testicular cells of Acrida furrita (Orthoptera: Acrididae). J. Invertebr. Pathel. 61, 15.CrossRefGoogle Scholar
Ndiaye, M.Mattei, X.Thiaw, O.T. (1995). Extracellular and intracellular rickettsia-like microorganisms in gonads of mosquitoes. J. Submicrosc. Cytal. Pathol. 27,557–63.Google ScholarPubMed
Petzelt, C., Hafner, M. (1989). Calcium and mitosis: mythos? In: The Cell Biology of Fertilization, Schatten, H. & Schatten, G.341–59. San Diego: Academic Press.CrossRefGoogle Scholar
Snyder, M. (1994). The spindle pole body of yeast. Chromosoma 103, 369–80.CrossRefGoogle ScholarPubMed
Thomso, H.M. (1960). A list and brief description of the microsporidia infecting insects. J. Insect Pathol. 2, 346–85.Google Scholar
Traut, W.Weith, A.Traut, C. (1986). Structural mutants he W chromosome in Ephestia (Insects, Lepidoptera). Genetica 7, 6979.Google Scholar
Vavra, J. (1988). Structure of the microsporidia.In Biology the Microsporidia Bulls, L.A..Cheng, T.C.185. New York: Plenum Press.Google Scholar
Whitaker, M.Patel, R. (1990). Calcium and cell cycle control. Development 108, 525–42.CrossRefGoogle ScholarPubMed
Winey, M.Byers, B. (1993). Assembly and function of the spindle pole body in budding yeast. Trends Genef J. Insect Pathol. 9,300–4.Google Scholar
Wolf, K.W. (1988). Cytology of Lepidoptera. Chromatinassociated, virus-like particles in testes of Pieris brassicae. Eur.J.Cell Biol. 47 137–7.Google Scholar
Wolf, K.W. (1990 a). Sheathed nuclear division in primary spermatocytea of Orgyia antiqua (Lepidoptera, Insects). BioSystems 24, 515.CrossRefGoogle Scholar
Wolf, K.W. (1990 b). Mitotic and meiotic spindles from two insect orders, Lepidoptera and Diptera, differ in terms of microtubule and membrane content. J. Cell Sci. 97,91100.CrossRefGoogle Scholar
Wolf, K.W. (1992). Spindle membranes and microtubules are coordinately reduced in apyrene relative to eupyrene spermatocytes of lnachio io (Lepidoptera, Nymphalidae). J. Submicrosc. Cytal. Pathol. 24, 381–94.Google Scholar
Wolf, K.W. (1994). The unique structure of Lepidopteran spindles. Int. Rev. Cytol. 152, 148.CrossRefGoogle Scholar
Wolf, K.W. (1995 a). Spindle membranes and spindle architecture in invertebrates. Micron 26, 6998.CrossRefGoogle Scholar
Wolf, K.W. (1995 b). The intraspindle membrane system of metaphase II spermatocytes in Phragmatebia fuliginosa (Lepideptera, Arctiidae) appears to form a continuum. J. Struct. Biol. 115, 41–9.CrossRefGoogle Scholar
Wolf, K.W. & Glatzel, S. (1996). Intracytoplasmic bacteria in male germ cells of Philudoria potaforia L. (Lasiocampidae, Lepidoptera, Insects). J. Invertebr. Pathol. 67, 279–88.CrossRefGoogle Scholar
Wolf, K.W. & Bastmeyer, M. (1991). Cytology of Lepidoptera. V. The Microtubule cytoskeleton in eupyrene spermatocytes of Ephestia kuehniella (Pyralidae), Machis io (Nymphalidae), and Orgyia antiqua (Lymantriidae). Eur. J. Cell Bisl. 55, 225–37.Google Scholar
Wolf, K.W. & Traut, W. (1991). Cytology of Lepidoptera. VII. The restructuring of eupyrene prophase i spermatocytes and its relationship to meiotic chromosome and spindle organization in Ephestia kuehniella. Z.Protoplasma 165,5163.CrossRefGoogle Scholar
Wolf, K.W., Baumgart, K. & Traut, W. (1987). Cytology of Lepidoptera. II. Fine structure of eupyrene and apyrene primary spermatocytes in Orgyia thyellina. Eur. J. Cell Biol. 44, 5767.Google Scholar
Wolniak, S.M. (1991). Patterns of regulation during mitosis. In The Cyfoskeletal Basis of Plant Growth and Form, ed. Lloyd, C.W. pp. 209–26. London: Academic Press.Google Scholar