Summary
The ultrastructure of freeze-substituted haustoria ofErysiphe graminis DC f. sp.hordei Marchal onHordeum vulgare L. cv. Villa is described. Freeze-substitution allows an improved visualization of thein vivo fine structure of haustoria of powdery mildews. The sheath membrane, as well as the profiles of the plasmalemma, nucleus, mitochondria, and vacuoles appear sharp and smoothly contoured. Invaginations are considered real features of the sheath membrane. Large vacuoles extending into the haustorial body and the haustorial lobes characterize older fungal structures. In the cytoplasm polyribosomes are homogeneously distributed whereas electron-dense glycogen-like inclusions are observed in the periphery of the cytoplasm. The rough endoplasmatic reticulum and the microtubules, primarily orientated with the longitudinal axis of the haustorium, are well resolved by means of the freeze-substitution technique. The method presented provides more detailed insight into the host-parasite interface under natural conditions.
Similar content being viewed by others
References
Bracker, C. E., 1967: Ultrastructure of fungi. Ann. Rev. Phytopathol.5, 343–374.
—, 1968: Ultrastructure of the haustorial apparatus ofErysiphe graminis and its relationship to the epidermal cell of barley. Phytopathology58, 12–30.
Bray, D. F., Wagenaar, E. B., 1978: A double staining technique for improved contrast of thin sections from Spurr-embedded tissue. Can. J. Bot.56, 129–132.
Bushnell, W. R., 1972: Physiology of fungal haustoria. Ann. Rev. Phytopathol.10, 151–176.
—,Dueck, J., Rowell, J. B., 1967: Living haustoria and hyphae ofErysiphe graminis f. sp.hordei with intact and partly dissected host cells ofHordeum vulgare. Can. J. Bot.45, 1719–1732.
—,Gay, J. L., 1978: Accumulation of solutes in relation to the structure and function of haustoria in powdery mildews. In: The powdery mildews (Spencer, D. M., ed.), pp. 183–235. New York: Academic Press.
De Bary, A., 1887: Comparative morphology and biology of the fungi, mycetezoa, and bacteria. Transl. by H. E. F.Garnsey and rev. by I. B.Balfour, 525 p. Oxford: Clarendon Press.
Ehrlich, H. G., Ehrlich, M. A., 1963: Electron microscopy of the sheath surrounding the haustorium ofErysiphe graminis. Phytopathology53, 1378–1380.
Gil, F., Gay, J. L., 1977: Ultrastructural and physiological properties of the host interfacial components of haustoria ofErysiphe pisi in vivo andin vitro. Physiol. Plant Pathol.10, 1–12.
Girbardt, M., 1969: Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma67, 413–441.
Grove, S. N., Bracker, C. E., 1970: Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J. Bacteriol.104, 989–1009.
Harvey, D. M. R., 1982: Freeze-substitution. J. Microsc.127, 209–221.
Hayat, M. A., 1981: Fixation for electron microscopy. New York: Academic Press.
Hazen, B. E., Bushnell, W. R., 1983: Inhibition of the hypersensitive reaction in barley to powdery mildew by heat shock and cytochalasin B. Physiol. Plant Pathol.23, 421–438.
Heath, I. B., Rethoret, K., Moens, P. B., 1984: The ultrastructure of mitotic spindles from conventionally fixed and freezesubstituted nuclei of the fungusSaprolegnia. Eur. J. Cell Biol.35, 284–295.
Hippe, S., 1984: Rapid cryofixation by a simple propane-double-jet device adapted to a modified specimen table of the BIOETCH 2005. Mikroskopie41, 289–301.
Hoch, H. C., Howard, R. J., 1980: Ultrastructure of freezesubstituted hyphae of the BasidiomyceteLaetisaria arvalis. Protoplasma103, 281–297.
—,Staples, R. C., 1983a: Ultrastructural organization of the nondifferentiated uredospore germling ofUromyces phaseoli varietytypica. Mycologia75, 795–824.
— —, 1983b: Visualization of actinin situ by rhodamine-conjugated phalloin in the fungusUromyces phaseoli. Eur. J. Cell Biol.32, 52–58.
Howard, R. J., 1980: Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton, and endomembranes after freeze-substitution. J. Cell Sci.48, 89–103.
—,Aist, J. R., 1979: Hyphal tip cell ultrastructure of the fungusFusarium: improved preservation by freeze-substitution. J. Ultrastruct. Res.66, 224–234.
——, 1980: Cytoplasmic microtubules and fungal morphogenesis: ultrastructural effects of methyl benzimidazole-2-ylcarbamate determined by freeze-substitution of hyphal tip cells. J. Cell Biol.87, 55–64.
Hunziker, E. B., Herrmann, W., Schenk, R. K., Mueller, M., Moor, H., 1984: Cartilage ultrastructure after high pressure freezing, freeze substitution, and low temperature embedding. I. Chondrocyte ultrastructure-implications for the theories of mineralization and vascular invasion. J. Cell Biol.98, 267–276.
Läuchli, A., Spurr, A. R., Wittkopp, R. W., 1970: Electron probe analysis of freeze-substituted, epoxy resin embedded tissue for ion transport studies in plants. Planta95, 341–350.
Manners, J. M., Gay, J. L., 1982: Transport, translocation and metabolism of14C-photosynthates at the host-parasite interface ofPisum sativum andErysiphe pisi. New Phytologist91, 221–244.
——, 1983: The host-parasite interface and nutrient transfer in biotrophic parasitism. In: Biochemical plant pathology (Callow, J. A., ed.), pp. 163–195. London: Wiley.
Martin, M., Gay, J. L., 1983: Ultrastructure of conidium development inErysiphe pisi. Can. J. Bot.61, 2472–2495.
Reynolds, E. S., 1963: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol.17, 208–212.
Spurr, A. R., 1969: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res.26, 31–43.
Stanbridge, B., Gay, J. L., Wood, R. K. S., 1971: Gross and fine structural changes inErysiphe graminis and barley before and during infection. In: Ecology of leaf surface micro-organisms (Preece, T. F., Dickinson, C. H., eds.), pp. 367–379. New York: Academic Press.
Steinbrecht, R. A., 1982: Experiments on freezing damage with freeze substitution using moth antaennae as test objects. J. Microsc.125, 187–192.
Uphoff, C., Raber, B. T., Cole, T. B., 1984: Tannic acid in routine staining of thin sections. J. Electron Microsc. Tech.1, 419–420.
Verna, A., 1983: A simple quick-freezing device for ultrastructure preservation: evaluation by freeze-substitution. Biol. Cell49, 95–98.
Weibull, C., Villiger, W., Carlemalm, E., 1984: Extraction of lipids during freeze-substitution ofAcholeplasma laidlawii cells for electron microscopy. J. Microsc.134, 213–216.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hippe, S. Ultrastructure of haustoria oferysiphe graminis f. sp.hordei preserved by freeze-substitution. Protoplasma 129, 52–61 (1985). https://doi.org/10.1007/BF01282305
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01282305