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Microtubules, organelle movement, and cross-wall formation at the sporangial-rhizoidal interface in the fungus,Chytridium confervae

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Summary

Chytridium confervae is a eucarpic, monocentric chytrid. We have used light and electron microscopy to study the relationship between the nutrient absorbing rhizoids and the asexually reproductive sporangium during growth. We have also examined the induction of zoosporogenesis by starvation, and subsequent differentiation until zoospore release. During growth the cytoplasm of the rhizoids and the developing sporangium was continuous and similar. At the start of starvation a bundle of fibers that were visible with light microscopy appeared at the junction between the rhizoids and the sporangium. Two hours after initiation of starvation a wall, that was also visible with light microscopy, formed to separate the rhizoids from the sporangium. Electron microscopy revealed a large, ordered array of microtubules in the thallus at the same time that the fibers appeared, and a sharp difference in the density of ribosomes in the cytoplasm of the sporangium and that of the rhizoids that was apparent immediately after starvation. This cytoplasmic difference was preserved by the formation of a cross-wall that was penetrated by plasmodesmata. After the wall was formed the cytoplasm of the rhizoids senesced. Comparison ofC. confervae with other organisms that use arrays of microtubules to move organelles is made and speculation on the role of the microtubules in organelle movement and wall formation inC. confervae is offered.

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References

  • Barr, D. J. S., 1970 a:Phlyctochytrium rienboldtae (Chytridiales): morphology and physiology. Canad. J. Bot.48, 479–484.

    Google Scholar 

  • —, 1970 b:Phlyctochytrium arcticum n. sp. (Chytridiales); morphology and physiology. Canad. J. Bot.48, 2279–2283.

    Google Scholar 

  • —, 1973: SixRhizophydium species (Chytridiales) in culture. Canad. J. Bot.51, 967–975.

    Google Scholar 

  • —, 1975: Morphology and zoospore discharge in single-pored, epibioticChytridiales. Canad. J. Bot.53, 164–178.

    Google Scholar 

  • Barstow, W. E., Lovett, J. S., 1974: Apical vesicles and microtubules in rhizoids ofBlastocladiella emersonii: effects of actinomycin D and cycloheximide on development during germination. Protoplasma82, 103–117.

    PubMed  Google Scholar 

  • — —, 1978: Ultrastructure of a reduced developmental cycle (minicycle) inBlastocladiella emersonii. Exp. Mycol.2, 145–155.

    Google Scholar 

  • Bennett, C. E., Stebbings, H., 1979: Redundant nutritive tubes in insect ovarioles: the fate of an extensive microtubule transport system. Cell Biol. Int. Rep.3, 577–583.

    PubMed  Google Scholar 

  • Burns, R. G., 1973:3H-colchicine binding. Failure to detect any binding to soluble proteins from various lower organisms. Exp. Cell Res.81, 285–292.

    PubMed  Google Scholar 

  • Burton, P. R., Fernandez, H. L., 1973: Delineation by lanthanum staining of filamentous elements associated with the surfaces of axonal microtubules. J. Cell Sci.12, 567–583.

    PubMed  Google Scholar 

  • Cantino, E. C., Hyatt, M. T., 1953: Phenotypic “sex” determination in the life history of a new species ofBlastocladiella, B. emersonii. Antonie van Leeuwenhoek19, 25–70.

    PubMed  Google Scholar 

  • Dales, S., 1963: Association between the spindle apparatus and reovirus. Proc. natl. Acad. Sci. (U.S.A.)50, 268–275.

    Google Scholar 

  • Davidse, L. C., 1973: Antimitotic activity of methyl benzimidazol-2-yl carbamate (MBC) inAspergillus nidulans. Pestic. Biochem. Physiol.3, 317–325.

    Google Scholar 

  • Dustin, P., 1978: Microtubules, 452 p. Berlin-Heidelberg-New York: Springer.

    Google Scholar 

  • Gaurlioff, L. P., Fuller, M. S., 1979: Morphological synchrony in axenic cultures ofChytridium confervae, a promising developmental system. Exp. Mycol.3, 3–15.

    Google Scholar 

  • Girbardt, M., 1968: Ultrastructure and dynamics of the moving nucleus. In: Aspects of Cell Motility. 22nd Symp. Soc. Exp. Biol. pp. 249–259 (Miller, P. L., ed.). London: Cambridge Univ. Press.

    Google Scholar 

  • Grove, S. N., 1978: The cytology of hyphal tip growth. In: The filamentous fungi. III. Developmental mycology (Smith, J. E., Berry, D. R., eds.), pp. 28–50. New York: J. Wiley and Sons.

    Google Scholar 

  • —, 1970: An ultrastructural basis for hyphal tip growth inPythium ultimum. Amer. J. Bot.57, 245–266.

    Google Scholar 

  • Gull, K., 1978: Form and function of septa in filamentous fungi. In: The filamentous fungi. III. Developmental mycology (Smith, J. E., Berry, D. R., eds.), pp. 78–93. New York: J. Wiley and Sons.

    Google Scholar 

  • Haber, J., Peloquin, J., Halvorson, H., Borisy, G., 1972: Colcemid inhibition of cell growth and the characterization of colcemid-binding activity inSaccharomyces cerevisiae. J. Cell Biol.55, 355–367.

    PubMed  Google Scholar 

  • Hawker, L. E., Gooday, M. A., 1967: Delimitation of the gametangia ofRhizopus sexualis (Smith) Callen: an electron microscope study of septum formation. J. gen. Microbiol.49, 371–376.

    Google Scholar 

  • — —,Bracker, C. E., 1966: Plasmodesmata in fungal cell walls. Nature212, 635.

    PubMed  Google Scholar 

  • Heath, I. B., 1974: A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J. theor. Biol.48, 445–449.

    PubMed  Google Scholar 

  • —, 1975 a: The effect of antimicrotubule agents on the growth and ultrastructure of the fungusSaprolegnia ferax and their ineffectiveness in disrupting hyphal microtubules. Protoplasma85, 147–176.

    PubMed  Google Scholar 

  • —, 1975 b: Colchicine and colcemid binding components of the fungusSaprolegnia ferax. Protoplasma85, 177–192.

    PubMed  Google Scholar 

  • —, ed., 1978: Nuclear division in the fungi, 235 p. New York: Academic Press.

    Google Scholar 

  • —,Heath, M. C., 1978: Microtubules and organelle movements in the rust fungusUromyces phaseoli var.vignae. Cytobiologie16, 393–411.

    PubMed  Google Scholar 

  • Hepler, P. K., Fosket, D. E., 1971: The role of microtubules in vessel member differentiation inColeus Protoplasma72, 213–236.

    Google Scholar 

  • —,Palevitz, B. A., 1974: Microtubules and microfilaments. Ann. Rev. Plant Physiol.25, 309–362.

    Google Scholar 

  • Hoch, H. C., 1977: Use of permanganate to increase electron opacity of fungal walls. Mycologia69, 1209–1213.

    PubMed  Google Scholar 

  • Hyams, J. S., Stebbings, H., 1977: The distribution and function of microtubules in nutritive tubes. Tissue and Cell9, 537–545.

    PubMed  Google Scholar 

  • Kloetzel, J, A., 1973: A simplified method of preparing optically clear flat embedments with epoxy resin. Stain Technol.48, 349–351.

    PubMed  Google Scholar 

  • Lembi, C. A., Morre, D. J., St.-Thompson., K., Hertel, R., 1971: N-1-Naphthylphthalamic-acid-binding activity of a plasma membrane-rich fraction from maize coleoptiles. Planta99, 37–45.

    Google Scholar 

  • Leslie, P. E., Lovett, J. S., 1968: Ultrastructural changes during sporangium formation and zoospore differentiation inBlastocladiella emersonii. Amer. J. Bot.55, 220–236.

    Google Scholar 

  • Luftig, R. B., Weihing, R. R., 1975: Adenovirus binds to rat brain microtubulesin vitro. J. Virol.16, 696–706.

    PubMed  Google Scholar 

  • MacGregor, H. C., Stebbings, H., 1970: A massive system of microtubules associated with cytoplasmic movement in telotrophic ovarioles. J. Cell Sci.6, 431–449.

    PubMed  Google Scholar 

  • Machlis, L., 1958: Evidence for a sexual hormone inAllomyces. Physiol. Plant.11, 181–192.

    Google Scholar 

  • McLaughlin, D. J., 1974: Ultrastructural localization of carbohydrate in the hymenium and subhymenium ofCoprinus. Evidence for the function of the Golgi apparatus. Protoplasma82, 341–364.

    PubMed  Google Scholar 

  • Malaisse, W. J., Malaisse-Lagae, F., Van Obberghen, E., Somers, G., Devis, G., Ravazzola, M., Orci, L., 1975: Role of microtubules in the phasic pattern of insulin release. Ann. N.Y. Acad. Sci.253, 630–652.

    PubMed  Google Scholar 

  • Morrison, P. J., 1977: Gametangial development inAllomyces macrogynus. I. The ultrastructure of early stages of development. Arch. Microbiol.113, 163–172.

    Google Scholar 

  • Murphy, D. B., Tilney, L. G., 1974: The role of microtubules in the movement of pigment granules in teleost melanophores. J. Cell Biol.61, 757–779.

    PubMed  Google Scholar 

  • Ochs, S., Sabri, M., Johnson, J., 1969: Fast transport system of materials in mammalian nerve fibers. Science163, 686–687.

    PubMed  Google Scholar 

  • Olson, L. W., 1972: Colchicine and the mitotic spindle of the aquatic phycomyceteAllomyces. Arch. Mikrobiol.84, 327–338.

    PubMed  Google Scholar 

  • —, 1973: A low molecular weight colchicine binding protein from the aquatic phycomyceteAllomyces neo-moniliformis. Arch. Mikrobiol.91, 281–286.

    Google Scholar 

  • Palevitz, B. A., Hepler, P. K., 1976: Cellulose microfibril orientation and cell shaping in developing guard cells ofAllium: The role of microtubules and ion accumulation. Planta132, 71–93.

    Google Scholar 

  • Pickett-Heaps, J. D., 1967: The effects of colchicine on the ultrastructure of dividing plant cells, xylem wall differentiation and distribution of cytoplasmic microtubules. Dev.Biol.15, 206–236.

    Google Scholar 

  • Powell, M. J., 1974: Fine structure of plasmodesmata in a chytrid. Mycologia66, 606–614.

    Google Scholar 

  • Raudaskoski, M., 1970: Occurrence of microtubules and microfilaments, and origin of septa in dikaryotic hyphae ofSchizophyllum commune. Protoplasma70, 415–422.

    Google Scholar 

  • —, 1972: Occurrence of microtubules in the hyphae ofSchizophyllum commune during intercellular nuclear migration. Arch. Microbiol.86, 91–100.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Robards, A. W., 1975: Plasmodesmata. Ann. Rev. Plant Physiol.26, 13–29.

    Google Scholar 

  • Rowley, J. C., III, Moran, D. T., 1975: A simple procedure for mounting wrinkle-free sections on formvar-coated slot grids. Ultramicroscopy1, 151–155.

    PubMed  Google Scholar 

  • Shibaoka, H., 1974: Involvement of wall microtubules in gibberellin promotion and kinetin inhibition of stem elongation. Plant Cell Physiol.15, 255–263.

    Google Scholar 

  • Smith, D. S., Järlfors, U., Cameron, B. F., 1975: Morphological evidence for the participation of microtubules in axonal transport. Ann. N.Y. Acad. Sci.253, 472–506.

    PubMed  Google Scholar 

  • Sparrow, F. K., jr., 1960: Aquatic Phycomycetes. Second edition. Ann Arbor: University of Michigan Press.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Stebbings, H., Hyams, J. S., 1979: Cell Motility, 192 p. London-New York: Longman.

    Google Scholar 

  • Steele, S. D., Fraser, T. W., 1973: The ultrastructure ofGeotrichum candidum hyphae. Canad. J. Microbiol.19, 1507–1512.

    Google Scholar 

  • Stempak, J. G., Ward, R. T., 1964: An improved staining method for electron microscopy. J. Cell Biol.22, 697–701.

    PubMed  Google Scholar 

  • Sternberger, L. A., 1974: Immunocytochemistry, 246 p. Englewood Cliffs, N.J.: Prentice-Hall.

    Google Scholar 

  • Takada, H., Yagi, T., Hiroaka, J., 1965: Elektronenoptische Untersuchungen anEndomycopsis fibuliger auf festen Nährböden. Protoplasma59, 494–505.

    Google Scholar 

  • Taylor, J. W.,Fuller, M. S., 1980: The Golgi apparatus and development of the zoospore discharge apparatus in the fungusChytridium confervae. Exp. Mycol. (in press).

  • —,Wells, K., 1979: A light and electron microscopic study of mitosis inBullera alba and the histochemistry of some cytoplasmic substances. Protoplasma98, 31–62.

    Google Scholar 

  • Thiéry, J.-P., 1967: Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J. Microsc.6, 987–1018.

    Google Scholar 

  • Wolff, J., Williams, J. A., 1973: The role of microtubules and microfilaments in thyroid secretion. Rec. Prog. Hor. Res.29, 229–295.

    Google Scholar 

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  1. Department of Botany, The University of Georgia, 30602, Athens, GA, USA

    J. W. Taylor & M. S. Fuller

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  1. J. W. Taylor
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Taylor, J.W., Fuller, M.S. Microtubules, organelle movement, and cross-wall formation at the sporangial-rhizoidal interface in the fungus,Chytridium confervae . Protoplasma 104, 201–221 (1980). https://doi.org/10.1007/BF01279768

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