1887

Abstract

Fruiting body formation in the basidiomycete is a developmental process that occurs as a response of the mycelium to external stimuli. First, localized, highly branched hyphal structures (knots) are formed as a reaction to nutritional depletion. Hyphal-knot formation is repressed by light; however, light signals are essential for the development of the hyphal knot into an embryonic fruiting body (primordium) as well as karyogamy, meiosis and fruiting body maturation. The role of the different environmental signals in the initial phases of fruiting body development was analysed. It was observed that two fungal galectins, Cgl1 and Cgl2, are differentially regulated during fruiting body formation. expression initiated in early stages of fruiting body development (hyphal knot formation) and was maintained until maturation of the fruiting body, whereas was specifically expressed in primordia and mature fruiting bodies. Immunofluorescence and immuno-electron microscopy studies detected galectins within specific fruiting body tissues. They localized in the extracellular matrix and the cell wall but also in membrane-bound bodies in the cytoplasm. Heterologous expression of Cgl2 in indicated that secretion of this protein occurred independently of the classical secretory pathway.

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2000-08-01
2019-09-16
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References

  1. Barondes, S. H., Cooper, D. N., Gitt, M. A. & Leffler, H. ( 1994; ). Galectins: structure and function of a large family of animal lectins. J Biol Chem 269, 20807-20810.
    [Google Scholar]
  2. Bejcek, B. E., Li, D. Y. & Deuel, T. F. ( 1989; ). Transformation by v-sis occurs by an internal autoactivation mechanism. Science 245, 1425-1499.
    [Google Scholar]
  3. Bickle, M., Delley, P. A., Schmidt, A. & Hall, M. N. ( 1998; ). Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J 17, 2235-2245.[CrossRef]
    [Google Scholar]
  4. Bottoli, A., Kertesz-Chaloupková, K., Boulianne, R. P., Granado, J. D., Aebi, M. & Kües, U. ( 1999; ). Rapid isolation of genes from an indexed library of C. cinereus in a novel pab1 +-cosmid. J Microbiol Methods 35, 129-141.[CrossRef]
    [Google Scholar]
  5. Brunelli, J. P. & Pall, M. L. ( 1993; ). A series of yeast shuttle vectors for expression of cDNAs and other DNA sequences. Yeast 9, 1299-1308.[CrossRef]
    [Google Scholar]
  6. Casselton, L. & Olesnicky, N. S. ( 1998; ). Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62, 55-70.
    [Google Scholar]
  7. Castle, A. J. & Boulianne, R. P. ( 1991; ). Fimbrial proteins of Ustilago violaceae, Coprinus cinereus, and Schizophyllum commune. MSA Newsletter 42, 8.
    [Google Scholar]
  8. Castle, A. J., Boulianne, R., Xu, J. & Day, A. W. ( 1992; ). Posttranslational modification of fimbrial protein from Ustilago violacea. Can J Microbiol 38, 1144-1149.[CrossRef]
    [Google Scholar]
  9. Celerin, M., Ray, J. M., Schisler, N. J., Day, A. W., Stetler-Stevenson, W. G. & Laudenbach, D. E. ( 1997; ). Fungal fimbriae are composed of collagen. EMBO J 15, 4445-4453.
    [Google Scholar]
  10. Charlton, S., Boulianne, R., Chow, Y. & Lu, B. C. ( 1992; ). Cloning and differential expression during the sexual cycle of a meiotic endonuclease-encoding gene from the basidiomycete Coprinus cinereus. Gene 122, 163-169.[CrossRef]
    [Google Scholar]
  11. Chomczynski, P. & Sacchi, N. ( 1987; ). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162, 156-159.
    [Google Scholar]
  12. Clémençon, H. (1997). Anatomie der Hymenomyceten: eine Einführung in die Cytologie und Plectologie der Krustenpilze, Porlinge, Keulenpilze, Leistlinge, Blätterpilze und Röhrlinge. Anatomy of the Hymenomycetes: an Introduction to the Cytology and Plectology of Crust Fungi, Bracket Fungi, Club Fungi, Chanterelles, Agarics and Boletes. Teufen, Switzerland: Flück-Wirth.
  13. Cleves, A. E., Cooper, D. N. W., Barondes, S. H. & Kelly, R. B. ( 1996; ). A new pathway for protein export in Saccharomyces cerevisiae. J Cell Biol 133, 1017-1026.[CrossRef]
    [Google Scholar]
  14. Cooper, D. N. W. & Barondes, S. H. ( 1990; ). Evidence for export of a muscle lectin from cytosol to extracellular matrix and for novel secretory mechanism. J Cell Biol 110, 1681-1691.[CrossRef]
    [Google Scholar]
  15. Cooper, D. N. W., Massa, S. M. & Barondes, S. H. ( 1991; ). Endogenous muscle lectin inhibits myoblast adherence to laminin. J Cell Biol 115, 1437-1448.[CrossRef]
    [Google Scholar]
  16. Cooper, D. N. W., Boulianne, R. P., Charlton, S., Farrell, E. M., Sucher, A. & Lu, B. C. ( 1997; ). Fungal galectins: sequence and specificity of two isolectins from Coprinus cinereus. J Biol Chem 272, 1514-1521.[CrossRef]
    [Google Scholar]
  17. Dunbar, C. E., Browder, T. M., Abrams, J. S. & Nienhuis, A. W. ( 1989; ). COOH-terminal-modified interleukin-3 is retained intra-cellularly and stimulates autocrine growth. Science 245, 1493-1496.[CrossRef]
    [Google Scholar]
  18. Eakle, K. A., Bernstein, M. & Emr, S. D. ( 1988; ). Characterization of a component of the yeast secretion machinery: identification of the SEC18 gene product. Mol Cell Biol 8, 4098-4109.
    [Google Scholar]
  19. Elliot, C. G. (1994). Reproduction in Fungi. London: Chapman & Hall.
  20. Franzusoff, A., Rothblatt, J. & Schekman, R. ( 1991; ). Analysis of polypeptide transit through the yeast secretory pathway. Methods Enzymol 194, 662-674.
    [Google Scholar]
  21. Gooday, G. W. ( 1975; ). The control of differentiation in fruit bodies of Coprinus cinereus. Rep Tottori Mycol Inst 12, 151-160.
    [Google Scholar]
  22. Gooday, G. W. ( 1982; ). Metabolic control of fruitbody morphogenesis in Coprinus cinereus. In Basidium and Basidiocarp, pp. 157-174. Edited by K. Wells & E. K. Wells. New York: Springer.
  23. Gooday, G. W. ( 1995; ). Cell walls. In The Growing Fungus, pp. 43-74. Edited by N. A. R. Gow & G. M. Gadd. London: Chapman & Hall.
  24. Granado, J., Kertesz-Chaloupková, K., Aebi, M. & Kües, U. ( 1997; ). Restriction enzyme-mediated DNA integration in Coprinus cinereus. Mol Gen Genet 256, 28-36.[CrossRef]
    [Google Scholar]
  25. Guillot, J. & Konska, G. ( 1997; ). Lectins in higher fungi. Biochem Syst Ecol 25, 203-230.[CrossRef]
    [Google Scholar]
  26. te Heesen, S., Janetzky, B., Lehle, L. & Aebi, M. ( 1992; ). The yeast WBP1 is essential for oligosaccharyltransferase activity in vivo and in vitro. EMBO J 11, 2071-2075.
    [Google Scholar]
  27. Hiscock, S. J. & Kües, U. ( 1999; ). Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int Rev Cytol 193, 165-295.
    [Google Scholar]
  28. Hughes, R. C. ( 1999; ). Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473, 172-185.[CrossRef]
    [Google Scholar]
  29. Ito, H., Fukuda, Y., Murata, K. & Kimura, A. ( 1983; ). Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153, 3153-3162.
    [Google Scholar]
  30. Jones, E. W. ( 1977; ). Bipartite structure of the ade3 locus of Saccharomyces cerevisiae. Genetics 85, 209-223.
    [Google Scholar]
  31. Kamada, T. ( 1994; ). Stipe elongation in fruit bodies. In The Mycota, vol. 1, Growth, Differentiation and Sexuality, pp. 367-379. Edited by J. G. H. Wessels & F. Meinhardt. Berlin: Springer.
  32. Kapteyn, J. C., Van Den Ende, H. & Klis, F. M. ( 1999; ). The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 1426, 373-383.[CrossRef]
    [Google Scholar]
  33. Kertesz-Chaloupková, K., Walser, P. J., Granado, J. D., Aebi, M. & Kües, U. ( 1998; ). Blue light overrides repression of asexual sporulation by mating-type genes in the basidiomycete Coprinus cinereus. Fungal Genet Biol 23, 95-109.[CrossRef]
    [Google Scholar]
  34. Kües, U. ( 2000; ). Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64, 316-353.[CrossRef]
    [Google Scholar]
  35. Kües, U., Granado, J. D., Hermann, R., Boulianne, R. P., Kertesz-Chaloupková, K. & Aebi, M. ( 1998; ). The A mating type and blue light regulate all known differentiation processes in the basidiomycete Coprinus cinereus. Mol Gen Genet 260, 81-91.[CrossRef]
    [Google Scholar]
  36. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef]
    [Google Scholar]
  37. Lu, B. C. ( 1974; ). Meiosis in Coprinus. V. The role of light on basidiocarp initiation, mitosis and hymenium differentiation in Coprinus lagopus. Can J Bot 52, 299-305.[CrossRef]
    [Google Scholar]
  38. Madelin, M. F. ( 1956a; ). The influence of light and temperature on fruiting of Coprinus lagopus Fr. in pure culture. Ann Bot 20, 467-480.
    [Google Scholar]
  39. Madelin, M. F. ( 1956b; ). Studies on the nutrition of Coprinus lagopus Fr., especially as affecting fruiting. Ann Bot 20, 307-330.
    [Google Scholar]
  40. Madelin, M. F. ( 1960; ). Visible changes in the vegetative mycelium of Coprinus lagopus Fr. at the time of fruiting. Trans Br Mycol Soc 43, 105-110.[CrossRef]
    [Google Scholar]
  41. Matsuo, T., Yamamoto, Y., Muraguchi, H. & Kamada, T. ( 1999; ). Effects of amino-acid substitutions in β-tubulin on benomyl sensitivity and microtubule functions in Coprinus cinereus. Mycoscience 40, 241-250.[CrossRef]
    [Google Scholar]
  42. Matthews, R. R. & Niederpruem, D. J. ( 1972; ). Differentiation in Coprinus lagopus. I. Control of fruiting and cytology of initial events. Arch Mikrobiol 87, 257-268.[CrossRef]
    [Google Scholar]
  43. May, G., Le Chevanton, L. & Pukilla, P. J. ( 1991; ). Molecular analysis of the Coprinus cinereus mating type A factor demonstrates an unexpectedly complex structure. Genetics 128, 529-538.
    [Google Scholar]
  44. Mehul, B. & Hughes, R. C. ( 1997; ). Plasma membrane targeting, vesicular budding and release of galectin 3 from the cytoplasm of mammalian cells during secretion. J Cell Sci 110, 1169-1178.
    [Google Scholar]
  45. Moore, D. ( 1981; ). Developmental genetics of Coprinus cinereus: genetic evidence that carpophores and sclerotia share a common pathway of initiation. Curr Genet 3, 145-150.[CrossRef]
    [Google Scholar]
  46. Moore, D. ( 1995; ). Tissue formation. In The Growing Fungus, pp. 423-466. Edited by N. A. R. Gow & G. M. Gadd. London: Chapman & Hall.
  47. Moore, D. (1998). Fungal Morphogenesis. Cambridge: Cambridge University Press.
  48. Moore, D. & Jirjis, R. I. ( 1976; ). Regulation of sclerotium production by primary metabolites in Coprinus cinereus. Trans Br Mycol Soc 66, 377-382.[CrossRef]
    [Google Scholar]
  49. Moore, D., Elhiti, M. M. Y. & Butler, R. D. ( 1979; ). Morphogenesis of the carpophore of Coprinus cinereus. New Phytol 66, 377-382.
    [Google Scholar]
  50. Moukha, S. M., Wösten, H. A. B., Asther, M. & Wessels, J. G. H. ( 1993; ). In situ localization of the secretion of lignin peroxidases in colonies of Phanerochaete chrysosporium using a sandwiched mode of culture. J Gen Microbiol 139, 969-978.[CrossRef]
    [Google Scholar]
  51. Ochieng, J., Leite-Browning, M. L. & Warfield, P. ( 1998; ). Regulation of cellular adhesion to extracellular matrix proteins by galectin-3. Biochem Biophys Res Commun 246, 788-791.[CrossRef]
    [Google Scholar]
  52. Qu, Z., Kayton, R. J., Ahmadi, P., Liebler, J. M., Powers, M. R., Planck, S. R. & Rosenbaum, J. T. ( 1998; ). Ultrastructural immunolocalization of basic fibroblast growth factor in mast cell secretory granules: morphological evidence for bFGF release through degranulation. J Histochem Cytochem 46, 1119-1128.[CrossRef]
    [Google Scholar]
  53. Rao, P. S. & Niederpruem, D. J. ( 1969; ). Carbohydrate metabolism during morphogenesis of Coprinus lagopus. J Bacteriol 100, 1222-1228.
    [Google Scholar]
  54. Reijnders, A. F. M. ( 1979; ). Developmental anatomy of Coprinus. Persoonia 10, 383-424.
    [Google Scholar]
  55. Rubartelli, A., Cozzolino, F., Talio, M. & Sitia, R. ( 1990; ). A novel secretory pathway for interleukin-1β, a protein lacking a signal sequence. EMBO J 9, 1503-1510.
    [Google Scholar]
  56. Rubartelli, A., Bajetto, A., Allavena, G., Wollman, E. & Sitia, R. ( 1992; ). Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 267, 24161-24164.
    [Google Scholar]
  57. Sasaki, T., Brakebusch, C., Engel, J. & Timpl, R. ( 1998; ). Mac-2 binding protein is a cell-adhesive protein of the extracellular matrix which self-assembles into ring-like structures and binds beta1 integrins, collagens and fibronectin. EMBO J 17, 1606-1613.[CrossRef]
    [Google Scholar]
  58. Sato, S., Burdett, I. & Hughes, C. ( 1993; ). Secretion of the baby hamster kidney 30-kDa galactose-binding lectin from polarized and nonpolarized cells: a pathway independent of the endoplasmic reticulum-golgi complex. Exp Cell Res 207, 8-18.[CrossRef]
    [Google Scholar]
  59. Seitz, L. C., Teliang, K., Cummings, W. J. & Zolan, M. E. ( 1996; ). The rad9 gene of Coprinus cinereus encodes a proline-rich protein required for meiotic chromosome condensation and synapsis. Genetics 142, 1105-1117.
    [Google Scholar]
  60. Swamy, S., Uno, I. & Ishikawa, T. ( 1984; ). Morphogenic effects of mutations at the A and B incompatibility factors in Coprinus cinereus. J Gen Microbiol 130, 3219-3224.
    [Google Scholar]
  61. Wang, H., Ng, T. B. & Ooi, V. E. C. ( 1998; ). Lectins from mushrooms. Mycol Res 102, 897-906.[CrossRef]
    [Google Scholar]
  62. Warfield, P. R., Makker, P. N., Raz, A. & Ochieng, J. ( 1997; ). Adhesion of human breast carcinoma to extracellular matrix proteins is modulated by galectin-3. Invasion Metastasis 17, 101-112.
    [Google Scholar]
  63. Wösten, H. A. B., Moukha, S. M., Sietsma, J. H. & Wessels, J. G. H. ( 1991; ). Localization of growth and secretion of proteins in Aspergillus niger. J Gen Microbiol 137, 2017-2023.[CrossRef]
    [Google Scholar]
  64. Yu, Z. X., Biro, S., Fu, Y. M., Sanchez, J., Smale, G., Sasse, J., Ferrans, V. J. & Casscells, W. ( 1993; ). Localization of basic fibroblast growth factor in bovine endothelial cells: immunohistochemical and biochemical studies. Exp Cell Res 204, 247-259.[CrossRef]
    [Google Scholar]
  65. Zolan, M. & Pukkila, P. ( 1986; ). Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6, 195-200.
    [Google Scholar]
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