Skip to main content
Log in

Intranuclear fibrillar material in cereal pollen mother cells

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Ultrastructural studies of cereal anthers found intranuclear bundles of microfilaments in pollen mother cells (PMCs) but not elsewhere. The ultrastructure, distribution, and behaviour of this fibrillar material (FM) are described. FM was seen in all 19 genotypes studied comprising Aegilops, Triticum, Secale, Hordeum and Avena species, which together included haploid, diploid and allo-and autopolyploid, and natural and synthetic polyploid examples. Detailed studies in diploid S. cereale, and hexaploid T. aestivum and Triticale showed that FM was present in PMC nuclei during premeiotic interphase, leptotene and zygotene but not at pachytene and later meiotic stages. Moreover, it was most abundant at late premeiotic interphase in T. aestivum, and at leptotene in S. cereale and Triticale, when it occurred in up to 100% of sampled PMC nuclei in an anther. Although FM and synaptonemal complex (SC) occurred together in some PMC nuclei at later stages, FM was present long before SC, and reached its peak of abundance before SC did. Bundles of FM often formed links at their ends between either two masses of chromatin, or more rarely, between chromatin and the nuclear membrane. Individual bundles of FM varied in length but showed roughly similar ranges of lengths and widths in these three species. They were up to about 0.2 μm in diameter and about 3 μm in length, equivalent to about 20% of the maximum diameter of the nuclei containing them. Reconstructions of PMC nuclei indicated that FM was never associated with centromeres but was sometimes, and perhaps usually, associated with telomeric or sub-telomeric chromosome segments.

The function of FM is unknown but its possible role is discussed in relation to (1) previously described intranuclear inclusions in meiocytes and (2) the cytogenetics and developmental behaviour of meiotic nuclei in the wheat comparium. As FM was a constant and characteristic structural component of PMC nuclei, its presence is probably of functional significance to the meiotic process. If so, it may function before, and over greater distances, than SC in establishing or maintaining the coorientation of chromosomes prerequisite for normal chromosome pairing. As FM was most abundant at stages when major chromosome movements occur, yet its distribution was non-centromeric, it is suggested that it may function in the attachment and movement of telomeres at the nuclear membrane formed after premeiotic mitosis. The possibility that a bundle of FM normally links corresponding sites on two homologues is considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bayliss, M.W., Riley, R.: An analysis of temperature-dependent asynapsis in Triticum aestivum. Genet. Res. Camb. 20, 193–200 (1972a)

    Google Scholar 

  • Bayliss, M.W., Riley, R.: Evidence of premeiotic control of chromosome pairing in Triticum aestivum. Genet. Res. Camb. 20, 201–212 (1972b)

    Google Scholar 

  • Bennett, M.D., Smith, J.B.: The effects of polyploidy on meiotic duration and pollen development in cereal anthers. Proc. roy. Soc. Lond. B, 181, 81–107 (1972)

    Google Scholar 

  • Bennett, M.D., Chapman, V., Riley, R.: The duration of meiosis in pollen mother cells of wheat, rye and Triticale. Proc. roy. Soc. Lond. B, 178, 259–175 (1971)

    Google Scholar 

  • Bennett, M.D., Rao, M.K., Smith, J.B., Bayliss, M.W.: Cell development in the anther, the ovule, and the young seed of Triticum aestivum L. var. Chinese Spring. Philos. Trans. R. Soc. Lond. B, 266, 39–81 (1973)

    Google Scholar 

  • Bennett, M.D., Stern, H., Woodward, M.: Chromatin attachment to nuclear membrane of wheat pollen mother cells. Nature (Lond.) 252, 395–396 (1974)

    Google Scholar 

  • Bogdanov, Y.F.: Formation of cytoplasmic synaptonemal-like polycomplexes at leptotene and normal synaptonemal complexes at zygotene in Ascaris suum male meiosis. Chromosoma (Berl.) 61, 1–21 (1977)

    Google Scholar 

  • Bottke, W.: Chromosome-associated paracrystalline nuclear inclusions in the spermatocytes of a pulmonate snail, Planorbarius corneus L. Chromosoma (Berl.) 55, 273–287 (1976)

    Google Scholar 

  • Bowman, J.G., Rajhathy, T.: Fusion of chromocentres in premeiotic interphase of Secale cereale and its possible relationship to chromosome pairing. Can. J. Genet. Cytol. 19, 313–321 (1977)

    Google Scholar 

  • Church, K., Moens, P.B.: Centromere behaviour during iuterphase and meiotic prophase in Allium fistulosum from 3-D, E.M. reconstruction. Chromosoma (Berl.) 56, 249–263 (1976)

    Google Scholar 

  • Comings, D.E.: The rationale for an ordered arrangement of chromatin in the interphase nucleus. Amer. J. hum. Genet. 20, 440–459 (1968)

    Google Scholar 

  • Dover, G.A.: The organisation and polarity of pollen mother cells of Triticum aestivum. J. Cell Sci. 11, 699–711 (1972)

    Google Scholar 

  • Dover, G.A., Riley, R.: The effect of spindle inhibitors applied before meiosis on meiotic chromosome pairing. J. Cell Sci. 12, 143–161 (1973)

    Google Scholar 

  • Dover, G.A., Riley, R.: Inferences from genetical evidence on the course of meiotic chromosome pairing in plants. Philos. Trans. R. Soc. Lond. B 277, 313–326 (1977)

    Google Scholar 

  • Driscoll, C.J., Darvey, N.L., Barber, H.N.: Effect of colchicine on meiosis in hexaploid wheat. Nature (Lond.) 216, 687–688 (1967)

    Google Scholar 

  • Fiil, A.: Oogenesis in the malaria mosquito Anopheles gambiae. Cell Tissue Res. 167, 23–35 (1976)

    Google Scholar 

  • Fiil, A., Moens, P.B.: The development, structure and function of modified synaptonemal complexes in mosquito oocytes. Chromosoma (Berl.) 41, 37–62 (1973)

    Google Scholar 

  • Feldman, M.: Regulation of somatic association and meiotic pairing in common wheat, pp. 169–178. In: Third Int. Wheat Genet. Symp. 1968

  • Feldman, M., Mello-Sampayo, T., Sears, E.R.: Somatic association in Triticum aestivum. Proc. Natl. Acad. Sci. USA 56, 1192–1199 (1966)

    Google Scholar 

  • Forer, A., Jackson, W.T.: Actin filaments in the endosperm mitotic spindles in a higher plant, Haemanthus katherinae Baker. Cytobiologie 12, 199–214 (1976)

    Google Scholar 

  • Franke, W.W., Heath, W., Van Der Woude, W.J., Morré, D.: Tubular and filamentous structures in pollen tubes: Possible involvement as guide elements in protoplasmic streaming and vectorial migration of secretory vesicles. Planta (Berl.) 105, 317–341 (1972)

    Google Scholar 

  • Fuge, H.: A crystalloid component in the meiotic spindle. Exp. Cell Res. 60, 309–313 (1970)

    Google Scholar 

  • Gillies, C.B.: The nature and extent of synaptonemal complex formation in haploid barley. Chromosoma (Berl.) 48, 441–453 (1974)

    Google Scholar 

  • Gillies, C.B.: An ultrastructural analysis of chromosomal pairing in maize. C. R. Trav. Lab. Carlsberg 40, 135–161 (1975)

    Google Scholar 

  • Gillies, C.B., Hyde, B.B.: Intranucleolar bodies in maize microsporocytes. Hereditas 74, 137–140 (1973)

    Google Scholar 

  • Gustafson, J.P., Bennett, M.D.: Preferential selection for wheat-rye substitutions in 42-chromosome triticale. Crop Sci. 16, 688–693 (1976)

    Google Scholar 

  • Hauser, M.: The intranuclear mitosis of the ciliates Paracineta limbata and Ichthyophthirius miltifilius. Chromosoma (Berl.) 36, 157–158 (1972)

    Google Scholar 

  • Ishikawa, H., Bischoff, R., Holtzer, H.: Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43, 312–328 (1969)

    Google Scholar 

  • Jaworska, H., Lima-de-Faria, A.: Multiple synaptonemal complexes at the region of gene amplification in Acheta. Chromosoma (Berl.) 28, 309–327 (1969)

    Google Scholar 

  • Kamiya, N.: Introductory remarks. In: Intern. cell biol. B.R. Brinkley, and K.R. Porter (eds.), pp. 361–366. New York: The Rockefeller University Press (1977)

    Google Scholar 

  • Karasaki, S.: Intranuclear crystal within the phagocytes. J. Cell Biol. 25, 654–660 (1965)

    Google Scholar 

  • Kasha, K.J., Burnham, C.R.: The location of interchange breakpoints in barley. II. Chromosome pairing and the intercross method. Can. J. Genet. Cytol. 7, 620–632 (1965)

    Google Scholar 

  • La Cour, L.F., Wells, B.: Some morphological aspects of the synaptonemal complex in higher plants. Philos. Trans. R. Soc. Lond. B 277, 259–266 (1977)

    Google Scholar 

  • Larter, E.N., Shebeski, L.H., McGinnis, R.C., Evans, L.E., Kaltsikes, P.J.: Rosner: A hexaploid triticale cultivar. Canad. J. Plant Sci. 50, 122–124 (1970)

    Google Scholar 

  • McFadden, E.S., Sears, E.R.: The origin of Triticum spelta and its free-threshing hexaploid relatives. J. Hered. 37, 81–89 (1946)

    Google Scholar 

  • McQuade, H.A., Bassett, B.: Synaptonemal complexes in premeiotic interphase of pollen mother cells of Triticum aestivum. Chromosoma (Berl.) 63, 153–159 (1977)

    Google Scholar 

  • O'Brien, T.P., Thimann, K.V.: Intracellular fibres in oat coleoptile cells and their possible significance in cytoplasmic streaming. Proc. Natl. Acad. Sci. USA 56, 888–894 (1966)

    Google Scholar 

  • Oliveira, L.: Ultrastructural, cytochemical and experimental studies on the cytoplasmic and nucleoplasmic inclusions of root meristematic cells of a Triticale. J. submicr. Cytol. 8, 29–39 (1976)

    Google Scholar 

  • Parthasarathy, M.V., Muhlethaler, K.: Ultrastructure of protein tubules in differentiating sieve elements. Cytobiologie 1, 17–36 (1969)

    Google Scholar 

  • Poux, N.: Sur l'existance de structures à arrangement périodique dans les cellules embryonnaires de Triticum vulgare Vill. (Graminées). J. Microsc. 2, 643–648 (1963)

    Google Scholar 

  • Rasmussen, S.W.: Ultrastructural studies of spermatogenesis in Drosophila melanogaster Meigen. Z. Zellforsch. 140, 125–144 (1973)

    Google Scholar 

  • Rasmussen, S.W.: Synaptonemal polycomplexes in Drosophila melanogaster. Chromosoma (Berl.) 49, 321–331 (1975)

    Google Scholar 

  • Reimer, L., Roessner, A., Themann, H., Bassewitz, D.B. v.: Optical diffraction on tilting series of paracrystalline intranuclear inclusions of dog liver parenchymal cells. J. Ultrastruct. Res. 45, 356–365 (1973)

    Google Scholar 

  • Reynold, E.S.: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Riley, R.: Cytogenetics of chromosome pairing. Genetics 78, 193–203 (1974)

    Google Scholar 

  • Riley, R., Kempana, C.: The homeologous nature of the non-homologous meiotic pairing in Triticum aestivum deficient for chromosome V (5B). Heredity 18, 287–306 (1963)

    Google Scholar 

  • Riley, R., Law, C.N.: Genetic variation in chromosome pairing. In Advanc. Genet. 13, 57–114 (1965)

    Google Scholar 

  • Riley, R., Unrau, J., Chapman, V.: Evidence on the origin of the B genome of wheat. J. Hered. 49, 91–98 (1958)

    Google Scholar 

  • Seïte, R.: Etude ultrastructurale de divers types d'inclusions nucléaires dans les neurones sympathiques du chat. J. Ultrastruct. Res. 30, 152–165 (1970)

    Google Scholar 

  • Smith, U., Smith, D.S.: A microtubular complex on the epidermal nucleus of an insect, Carausius morosus. J. Cell Biol. 26, 961–967 (1965)

    Google Scholar 

  • Spurr, A.R.: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43 (1969)

    Google Scholar 

  • Srivastava, L.M., O'Brien, T.P.: On the ultrastructure of cambium and its vascular derivatives. Protoplasma 61, 257–276 (1966)

    Google Scholar 

  • Taylor, D.L.: Dynamics of cytoplasmic structure and contractility. In: Int. cell biology (B.R. Brinkley and K.R. Porter, eds.), pp. 367–377. New York: The Rockefeller University Press 1977

    Google Scholar 

  • Thomas, J.B., Kaltsikes, P.J.: A bouquet-like attachment plate for telomeres in leptotene of rye revealed by heterochromatin staining. Heredity 36, 155–162 (1976)

    Google Scholar 

  • Vivier, E., André, J.: Existance d'inclusions d'ultrastructure fibrillaire dans le macronucleus de certaines souches de Paramecium caudatum Ehr. C.R. Acad. Sci. (Paris) 252, 1848–1853 (1961)

    Google Scholar 

  • Weber, K.: Specific visualization of tubulin containing structures by immunofluorescence microscopy: cytoplasmic microtubules, vinblastine induced paracrystals and mitotic figures. In: Microtubules and microtubule inhibitors (M, Borgers, and M. de Brabander, eds.), pp. 313–325. Amsterdam: Publication Comp. North Holland. 1975

    Google Scholar 

  • Wells, B.: A convenient technique for the collection of ultra-thin sections. Micron 5, 79–81 (1974)

    Google Scholar 

  • Welsch, B.: Synaptonemal complex und Chromosomenstruktur in der achiasmatischen Spermatogenese von Panorpa communis. Chromosoma (Berl.) 43, 19–74 (1974)

    Google Scholar 

  • Wenzel, G., Hoffmann, F., Thomas, E.: Increased induction and chromosome doubling of androgenetic haploid rye. Theor. Appl. Genet. 51, 81–86 (1977)

    Google Scholar 

  • Wergin, W.P., Gruber, P.J., Newcomb, E.H.: Fine structural investigation of nuclear inclusions in plants. J. Ultrastr. Res. 30, 533–557 (1970)

    Google Scholar 

  • Westergaard, M., Wettstein, D. von: Studies on the mechanism of crossing over. IV. The molecular organisation of the synaptinemal complex in Neottialla (Cooke) Saccardo (Ascomycetes). C.R. Trav. Lab. Carlsberg 37, 239–268 (1970)

    Google Scholar 

  • Westergaard, M., Wettstein, D. von: The synaptinemal complex. Annu. Rev. Genet. 6, 71–110 (1972)

    Google Scholar 

  • Wettstein, D. von: The assembly of the synaptinemal complex. Phil. Trans. roy. Soc. Lond. B 277, 235–243 (1977)

    Google Scholar 

  • Zee, S.Y., Chambers, T.C.: Fine structure of the primary root phloem of Pisum. Aust. J. Both. 16, 37–47 (1968)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bennett, M.D., Smith, J.B., Simpson, S. et al. Intranuclear fibrillar material in cereal pollen mother cells. Chromosoma 71, 289–332 (1979). https://doi.org/10.1007/BF00287138

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00287138

Keywords

Navigation