Molecular Organization and Construction of the Fungal Cell Wall

  • Hans De Nobel
  • J. Hans Sietsma
  • Herman Van Den Ende
  • Frans M. Klis
Part of the The Mycota book series (MYCOTA, volume 8)

Abstract

The fungal wall accounts for about 20–30% of the cellular dry weight and thus represents a major investment for the cell in terms of metabolic energy. It is responsible for the shape of the cell, offers protection against mechanical damage, and functions as a molecular sieve. Furthermore, it may contain adhesive proteins involved in bundling hyphae into macroscopic structures, in recognizing mating partners or host cells, or in binding to the substratum. Cell wall proteins may also confer hydrophobic properties to the cell surface. Various reviews and books have discussed the fungal cell wall and its properties (Kuhn et al. 1990; Peberdy 1990; Fleet 1991; Ruiz-Herrera 1992; Sentandreu et al. 1994; Sietsma and Wessels 1994; Wessels 1994; Gooday 1995; for earlier work see Wessels and Sietsma 1981). In this review, we will focus on recent developments and try to present them against the background of older work.

Keywords

Polysaccharide Enzymatic Degradation Fibril Oligosaccharide Maltosa 

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References

  1. Arellano M, Duran A, Perez P (1996) Rho 1 GTPase activates the (1–3)beta-d-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15:4584–4591PubMedGoogle Scholar
  2. Baba M, Osumi M (1987) Transmission and scanning electron microscopic examination of intracellular organelles in freeze-substituted Kloeckera and Saccharomyces cerevisiae yeast cells. J Electron Microsc Tech 5:249–261CrossRefGoogle Scholar
  3. Bacon JSD, Jones D, Farmer VC, Webley DM (1968) The occurrence of α-(1–3)-glucan in Cryptococcus, Schizosaccharomyces and Polyporus species and its hydrolysis by a streptomycete culture filtrate lysing cell walls of Cryptococcus. Biochim Biophys Acta 158:313–315PubMedCrossRefGoogle Scholar
  4. Bago B, Chamberland H, Goulet A, Vierheilig H, Lafontaine J-G, Piché E (1996) Effect of nikkomycin Z, a chitin synthase inhibitor, on hyphal growth and cell wall structure of two arbuscular-mycorrhizal fungi. Protoplasma 192:80–92CrossRefGoogle Scholar
  5. Bailey DA, Feldmann PJ, Bovey M, Gow NA, Brown AJ (1996) The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J Bacteriol 178:5353–5360PubMedGoogle Scholar
  6. Barkai-Golan R, Mirelman D, Sharon N (1978) Studies on growth inhibition by lectins of Penicillia and Aspergilli. Arch Microbiol 116:119–124PubMedCrossRefGoogle Scholar
  7. Barran LR, Schneider EF, Wood PJ, Madhosingh C, Miller RW (1975) Cell wall of Fusarium sulphureum. I. Chemical composition of the hyphal cell wall. Biochim Biophys Acta 392:148–158PubMedCrossRefGoogle Scholar
  8. Bartnicki-Garcia S, Persson J, Chanzy H (1994) An electron microscope and electron diffraction study of the effect of Calcofluor and Congo Red on the biosynthesis of chitin in vitro. Arch Biochem Biophys 310:6–15PubMedCrossRefGoogle Scholar
  9. Bell-Pedersen D, Dunlap JC, Loros JJ (1992) The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of the conidial rodlet layer. Genes Dev 6:2382–2394PubMedCrossRefGoogle Scholar
  10. Benitez T, Villa TG, Acha IG (1976) Effects of polyoxin D on germination, morphological development and biosynthesis of the cell wall of Trichoderma viride. Arch Microbiol 108:183–188PubMedCrossRefGoogle Scholar
  11. Boone C, Sommer SS, Hensel A, Bussey H (1990) Yeast KRE genes provide evidence for a pathway of cell wall beta-glucan assembly. J Cell Biol 110:1833–1843PubMedCrossRefGoogle Scholar
  12. Boone C, Sdicu A, Laroche M, Bussey H (1991) Isolation from Candida albicans of a functional homolog of the Saccharomyces cerevisiae KRE1 gene, which is involved in cell wall beta-glucan synthesis. J Bacteriol 173:6859–6364PubMedGoogle Scholar
  13. Borgia PT, Iartchouk N, Riggle PJ, Winter KR, Koltin Y, Bulawa CE (1996) The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet Biol 20:193–203PubMedCrossRefGoogle Scholar
  14. Bowen AR, Chen-Wu JL, Momany M, Young R, Szaniszlo PJ, Robbins PW (1992) Classification of fungal chitin synthases. Proc Natl Acad Sci USA 89:519–523PubMedCrossRefGoogle Scholar
  15. Broekaert WF, Van Parijs J, Leyns F, Joos H, Peumans WJ (1989) A chitin-binding lectin from stinging nettle rhizomes with antifungal properties. Science 245: 1100–1102PubMedCrossRefGoogle Scholar
  16. Brown JL, Bussey H (1993) The yeast KRE9 gene encodes an O-glycoprotein involved in cell surface beta-glucan assembly. Mol Cell Biol 13:6346–6356PubMedGoogle Scholar
  17. Brul S, King A, Van Der Vaart JM, Chapman J, Klis F, Verrips CT (1997) The incorporation of mannoproteins in the cell wall of S. cerevisiae and filamentous Ascomycetes. Antonie van Leeuwenhoek 72:229–237PubMedCrossRefGoogle Scholar
  18. Bulawa CE (1993) Genetics and molecular biology of chitin synthesis in fungi. Annu Rev Microbiol 47:505–534PubMedCrossRefGoogle Scholar
  19. Bulawa CE, Slater M, Cabib E, Au-Young J, Sburlati A, Adair WL Jr, Robbins PW (1986) The S. cerevisiae structural gene for chitin synthase is not required for chitin synthesis in vivo. Cell 46 213–225PubMedCrossRefGoogle Scholar
  20. Cabib E, Drgonova J, Drgon T (1998) Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307–333PubMedCrossRefGoogle Scholar
  21. Cao L, Chan CM, Lee C, Wong SS, Yuen KY (1998) MP1 encodes an abundant and highly antigenic cell wall mannoprotein in the pathogenic fungus Penicillium marneffei. Infect Immun 66:966–973PubMedGoogle Scholar
  22. Cappellaro C, Mrsa V, Tanner W (1998) New potential cell wall glucanases of Saccharomyces cerevisiae and their involvement in mating. J Bacteriol 180:5030–5037PubMedGoogle Scholar
  23. Caro LH,Tettelin H, Vossen JH, Ram AF, van den Ende H, Klis FM (1997) In silicio identification of glycosylphosphatidyl inositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477–89PubMedCrossRefGoogle Scholar
  24. Casanova M, Lopez-Ribot JL, Martinez JP, Sentandreu R (1992) Characterization of cell wall proteins from yeast and mycelial cells of Candida albicans by labeling with biotin: comparison with other techniques. Infect Immun 60:4898–4906PubMedGoogle Scholar
  25. Chuang JS, Schekman RW (1996) Differential trafficking and timed localisation of two chitin synthase proteins, Chs2p and Chs3p. J Cell Biol 135:597–610PubMedCrossRefGoogle Scholar
  26. Cormack BP, Ghori N, Falkow S (1999) An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578–582PubMedCrossRefGoogle Scholar
  27. Costanzo MC, Hogan JD, Cusick ME, Davis BP, Fancher AM, Hodges PE, Kondu P, Lengieza C, Lew-Smith JE, Linger C, Roberg-Perez KJ, Tillberg M, Brooks JE, Garreis JI (2000) The yeast proteome database (YPD) and Caenorhabditis elegans proteome database (WormPD): comprehensive resources for the organization and comparison of model organism protein information. Nucleic Acids Res 28:73–76PubMedCrossRefGoogle Scholar
  28. Dallies N, Francois J, Paquet V (1998) A new method for quantitative determination of polysaccharides in the yeast cell wall. Application to the cell wall defective mutants of Saccharomyces cerevisiae. Yeast 14:1297–1306PubMedCrossRefGoogle Scholar
  29. Dean N (1999) Asparagine-linked glycosylation in the yeast Golgi. Biochim Biophys Acta 1426:309–322PubMedCrossRefGoogle Scholar
  30. De Nobel JGH, Barnett JA (1991) Passage of molecules through yeast cell walls: a brief essay-review. Yeast 7:313–323PubMedCrossRefGoogle Scholar
  31. De Nobel JG, Lipke PN (1994) Is there a role for GPIs in yeast cell-wall assembly? Trends Cell Biol 4:42–45PubMedCrossRefGoogle Scholar
  32. De Nobel JG, Dijkers C, Hooijberg E, Klis FM (1989) Increased cell wall porosity in Saccharomyces cerevisiae after treatment with dithiothreitol and EDTA. J Gen Microbiol 135:2077–2084Google Scholar
  33. De Nobel JG, Klis FM, Priem J, Munnik T, Van Den Ende H (1990) The glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cervisiae. Yeast 6:491–499PubMedCrossRefGoogle Scholar
  34. Dijkgraaf GJ, Brown JL, Bussey H (1996) The KNH1 gene of Saccharomyces cerevisiae is a functional homolog of KRE9. Yeast 12:683–692PubMedCrossRefGoogle Scholar
  35. Domer JE, Hamilton JG, Harkin JC (1967) Comparative study of the cell walls of the yeastlike and mycelial phases of Histoplasma capsulatum. J Bacteriol 94:466–474PubMedGoogle Scholar
  36. Douglas CM, D’Ippolito JA, Shei GJ, Meinz M, Onishi J, Marrinan JA, Li W, Abruzzo GK, Flattery A, Bartizal K, Mitchell A, Kurtz MB (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-d-glucan synthase inhibitors. Antimicrob Agents Chemother 41:2471–2479PubMedGoogle Scholar
  37. Drgonova J, Drgon T, Tanaka K, Kollar R, Chen GC, Ford RA, Chan CS,Takai Y, Cabib E (1996) Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272:277–279PubMedCrossRefGoogle Scholar
  38. Dugger KO, Villareal KM, Ngyuen A, Zimmermann CR, Law JH, Galgiani JN (1996) Cloning and sequence analysis of the cDNA for a protein from Coccidioides immitis with immunogenic potential. Biochem Biophys Res Commun 218:485–489PubMedCrossRefGoogle Scholar
  39. Elorza MV, Rico H, Sentandreu R (1983) Calcofluor White alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. J Gen Microbiol 129:1577–1582PubMedGoogle Scholar
  40. Fèvre M, Girard V, Nodet P (1990) Cellulose and β-glucan synthesis in Saprolegnia. In: Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (eds) Biochemistry of cell walls and membranes in fungi. Springer, Berlin Heidelberg New York, pp 97–107CrossRefGoogle Scholar
  41. Fleet GH (1991) Cell walls. In: Rose AH, Harrison JS (eds) The yeasts, 2nd edn, vol 4. Yeast organelles. Academic Press, London, pp 199–277Google Scholar
  42. Fleet GH, Phaff HJ (1981) Fungal glucans. Structure and metabolism. In: Tanner W, Loewus FA (eds) Encyclopedia of plant physiology, vol 13B. Plant carbohydrates II, extracellular carbohydrates. Springer, Berlin Heidelberg New York, pp 416–440CrossRefGoogle Scholar
  43. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, Lemoine J, Vorgias CE, Diaquin M, Latgé J-P (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275:27594–27607PubMedGoogle Scholar
  44. Fonzi WA (1999) PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of beta-1,3- and beta-1,6-glucans. J Bacteriol 181:7070–7079PubMedGoogle Scholar
  45. Frost DJ, Brandt KD, Cugier D, Goldman R (1995) A whole-cell Candida albicans assay for the detection of inhibitors towards fungal cell wall synthesis and assembly. J Antibiot (Tokyo) 48:306–310CrossRefGoogle Scholar
  46. Fujii T, Shimoi H, Iimura Y (1999) Structure of the glucan-binding sugar chain of Tip1p, a cell wall protein of Saccharomyces cerevisiae. Biochim Biophys Acta 1427:133–144PubMedCrossRefGoogle Scholar
  47. Gaur NK, Klotz SA (1997) Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun 65:5289–5294PubMedGoogle Scholar
  48. Gemmili TR, Trimble RB (1999) Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim Biophys Acta 1426:227–237CrossRefGoogle Scholar
  49. Goldman RC, Sullivan PA, Zakula D, Capobianco JO (1995) Kinetics of beta-1,3-glucan interaction at the donor and acceptor sites of the fungal glucosyltransferase encoded by the BGL2 gene. Eur J Biochem 227:372–378PubMedCrossRefGoogle Scholar
  50. Gooday GW (1971) An autoradiographic study of hyphal growth of some fungi. J Gen Microbiol 67:125–133Google Scholar
  51. Gooday GW (1990) Inhibition of chitin metabolism. In: Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (eds) Biochemistry of Cell Walls and Membranes in Fungi. Springer, Berlin Heidelberg New York, pp 61–79CrossRefGoogle Scholar
  52. Gooday GW (1995) Cell walls. In: Gow NAR, Gadd GM (eds) The Growing Fungus. Chapman and Hall, London, pp 43–62CrossRefGoogle Scholar
  53. Gooday GW, Schofield DA (1995) Regulation of chitin synthesis during growth of fungal hyphae: the possible participation of membrane stress. Can J Bot 73 [Suppl 1]:S114–S121CrossRefGoogle Scholar
  54. Gozalbo D, Dubon F, Schwenke J, Sentandreu R (1987) Characterization of chitosomes in Candida albicans protoplasts. Exp Mycol 11:331–337CrossRefGoogle Scholar
  55. Gozalbo D, Dubon F, Sentandreu R (1992) Chitin synthetase activity is bound to the plasma membrane and to a cytoplasmic particulate fraction in Candida albicans germ tube cells. FEMS Microbiol Lett 97:255–259CrossRefGoogle Scholar
  56. Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62:1264–1300PubMedGoogle Scholar
  57. Hamada K, Terashima H, Arisawa M, Kitada K (1998) Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J Biol Chem 9:26946–26953CrossRefGoogle Scholar
  58. Hamada K, Terashima H, Arisawa M, Yabuki N, Kitada K (1999) Amino acid residues in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J Bacteriol 181:3886–3889PubMedGoogle Scholar
  59. Haplová J, Farkas V, Hejtmánek M, Kodousek R, Malinsky J (1994) Effect of the new fluorescent brightener Rylux BSU on morphology and biosynthesis of cell walls in Saccharomyces cerevisiae. Arch Microbiol 161:340–344PubMedGoogle Scholar
  60. Hartland RR Emerson GW, Sullivan PA (1991) A secreted β-glucan-branching enzyme from Candida albicans. Proc R Soc Lond B Biol Sci 246:155–160CrossRefGoogle Scholar
  61. Hartland RP, Vermeulen CA, Klis FM, Sietsma JH, Wessels JG (1994) The linkage of (1–3)-beta-glucan to chitin during cell wall assembly in Saccharomyces cerevisiae. Yeast 10:1591–1599PubMedCrossRefGoogle Scholar
  62. Hartland RP, Fontaine T, Debeaupuis J-P, Simenel C, Delepierre M, Latgé J-P (1996) A novel β-(1–3)-glucanosyltransferase from the cell wall of Aspergillus fumigatus. J Biol Chem 271:26843–26849PubMedCrossRefGoogle Scholar
  63. Hearn VM, Sietsma JH (1994) Chemical and immunological analysis of the Aspergillus fumigatus cell wall. Microbiology 140:789–795PubMedCrossRefGoogle Scholar
  64. Heath IB (1994) The cytoskeletoe. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol 1. Springer, Berlin Heidelberg New York, pp 43–65Google Scholar
  65. Hector RF (1993) Compounds active against cell walls of medically important fungi. Clin Microbiol Rev 6:1–21PubMedGoogle Scholar
  66. Herscovics A (1999) Processing glycosidases of Saccharomyces cerevisiae. Biochim Biophys Acta 1426: 275–286PubMedCrossRefGoogle Scholar
  67. Herrero E, Boyd A (1986) Mannoproteins from the cell wall of Kluyveromyces lactis. FEMS Microbiol Lett 36:207–211CrossRefGoogle Scholar
  68. Herrero E, Sanz P, Sentandreu R (1987) Cell wall proteins liberated by zymolyase from several ascomycetous and imperfect yeasts. J Gen Microbiol 133:2895–2903Google Scholar
  69. Hochstenbach F, Klis FM, Van Den Ende H, Van Donselaar E, Peters PJ, Klausner RD (1998) Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc Natl Acad Sci USA 95:9161–9166PubMedCrossRefGoogle Scholar
  70. Hogan LH, Klein BS (1994) Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62:3543–3546PubMedGoogle Scholar
  71. Horisberger M, Rouvet-Vauthey M (1985) Cell wall architecture of the fission yeast Schizosaccharomyces pombe. Experientia 41:748–750CrossRefGoogle Scholar
  72. Horiuchi H, Fujiwara M, Yamashita S, Ohta A, Takagi M (1999) Proliferation of intrahyphal hyphae caused by disruption of csmA, which encodes a class V chitin synthase with a myosin motor-like domain in Aspergillus nidulans. J Bacteriol 181:3721–3729PubMedGoogle Scholar
  73. Howard RJ, Aist JR (1979) Hyphal tip cell ultrastructure of the fungus Fusarium :improved preservation by freeze-substitution. J Ultrastruct Res 66:24–234CrossRefGoogle Scholar
  74. Hoyer LL, Hecht JE (2000) The ALS6 and ALS7 genes of Candida albicans. Yeast 16:847–855PubMedCrossRefGoogle Scholar
  75. Hoyer LL, Scherer S, Shatzman AR, Livi GP (1995) Candida albicans ALS1: domains related to a Saccharomyces cerevisiae sexual agglutinin separated by a repeating motif. Mol Microbiol 15:39–54PubMedCrossRefGoogle Scholar
  76. Hoyer LL, Payne TL, Hecht JE (1998a) Identification of Candida albicans ALS2 and ALS4 and localization of Als proteins to the fungal cell surface. J Bacteriol 180:5334–5343PubMedGoogle Scholar
  77. Hoyer LL, Payne TL, Bell M, Myers AM, Scherer S (1998b) Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet 33:451–459PubMedCrossRefGoogle Scholar
  78. Hunsley D, Burnett JH (1970) Ultrastructural architecture of the walls of some hyphal fungi. J Gen Microbiol 62:203–218Google Scholar
  79. Hunsley D, Kay D (1976) Wall structure of the Neurospora hyphal apex: immunofluorescent localization of wall surface antigens. J Gen Microbiol 95:233–248Google Scholar
  80. Hwang CS, Kolattukudy PE (1995) Isolation and characterization of genes expressed uniquely during appres-sorium formation by Colletotrichum glueosporioides conidia induced by the host surface wax. Mol Gen Genet 247:282–294PubMedCrossRefGoogle Scholar
  81. Ishiguro J, Saitou A, Duran A, Ribas JC (1997) cps1+, a Schizosaccharomyces pombe gene homolog of Saccharomyces cerevisiae FKS genes whose mutation confers hypersensitivity to cyclosporin A and papula-candin B. J Bacteriol 179:7653–7662PubMedGoogle Scholar
  82. Jelsma J, Kreger DR (1975) Ultrastructural observation on (1–3)-β-d-glucan from fungal cell walls. Carbohydr Res 43:200–203PubMedCrossRefGoogle Scholar
  83. Jentoft N (1990) Why are proteins O-glycosylated? Trends Biochem Sci 15:291–294PubMedCrossRefGoogle Scholar
  84. Jikibara T, Takegawa K, Iwahara S (1992) Studies on the uronic acid-containing glycoproteins of Fusarium sp. M7–1. III. The primary structures of the acidic polysaccharides of the glycoproteins. J Biochem 111:236–243PubMedGoogle Scholar
  85. Jung US, Levin DE (1999) Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol Microbiol 34:1049–1057PubMedCrossRefGoogle Scholar
  86. Kanetsuna F, Carbonell LM (1970) Cell wall glucans of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 101:675–681PubMedGoogle Scholar
  87. Kanetsuna F, Carbonell LM (1971) Cell wall composition of the yeast-like and mycelial forms of Blastomyces dermatitidis. J Bacteriol 106:946–953PubMedGoogle Scholar
  88. Kapteyn JC, Montijn RC, Vink E, De La Cruz J, Llobell A, Douwes JE, Shimoi H, Lipke PN, Klis FM (1996) Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked β-1,3/β-1,6-glucan heteropolymer. Glycobiology 6:337–345PubMedCrossRefGoogle Scholar
  89. Kapteyn JC, Ram AFJ, Groos EM, Kollar R, Montijn RC, Van Den Ende H, Llobell A, Cabib E, Klis FM (1997) Altered extent of cross-linking of beta 1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall beta-1,3-glucan content. J Bacteriol 179:6279–6284PubMedGoogle Scholar
  90. Kapteyn JC, Van Den Ende H, Klis FM (1999a) The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 6:373–383CrossRefGoogle Scholar
  91. Kapteyn JC, Van Egmond P, Sievi E, Van Den Ende H, Makarow M, Klis FM (1999b) The contribution of the O-glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild-type cells and beta-1,6-glucan-deficient mutants. Mol Microbiol 31: 1835–1844PubMedCrossRefGoogle Scholar
  92. Kapteyn JC, Hoyer LL, Hecht JE, Müller WH, Verkley AJ, Andel A, Makarow M, Van Den Ende H, Klis FM (2000) The cell wall architecture of Candida albicans wild-type cells and cell-wall-defective mutants. Mol Microbiol 35:601–611PubMedCrossRefGoogle Scholar
  93. Katayama S, Hirata D, Arellano M, Pérez P,Toda T (1999) Fission yeast α-glucan synthase Mok1 requires the actin cytoskeleton to localize the sites of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function. J Cell Biol 144:1173–1186PubMedCrossRefGoogle Scholar
  94. Kelly R, Register E, Hsu MJ, Kurtz M, Nielsen J (1996) Isolation of a gene involved in β-1,3-glucan synthesis in Aspergillus nidulans and purification of the corresponding protein. J Bacteriol 178:4381–4391PubMedGoogle Scholar
  95. Ketela T, Green R, Bussey H (1999) Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J Bacteriol 181:3330–3340PubMedGoogle Scholar
  96. Klebl F, Tanner W (1989) Molecular cloning of a cell wall exo-beta-1,3-glucanase from Saccharomyces cerevisiae. J Bacteriol 171:6259–6264PubMedGoogle Scholar
  97. Klimpel KR, Goldman WE (1988) Cell walls from avirulent variants of Histoplasma capsulatum lack alpha-(1,3)-glucan. Infect Immun 56:2997–3000PubMedGoogle Scholar
  98. Klis FM, Ram AFJ, Montijn RC, Kapteyn JC, Caro LHP, Vossen JH, Van Berkel MAA, Brekelmans SSC, Van Den Ende H (1998) Posttranslational modifications of secretory proteins. Methods Microbiol 26:224–238Google Scholar
  99. Knauer R, Lehle L (1999) The oligosaccharyltransferase complex from yeast. Biochim Biophys Acta 1426:259–274PubMedCrossRefGoogle Scholar
  100. Kollár R, Petrakova E, Ashwell G, Robbins PW, Cabib E (1995) Architecture of the yeast cell wall: the linkage between chitin and β-1,3-glucan. J Biol Chem 270: 1170–1178PubMedCrossRefGoogle Scholar
  101. Kollár R, Reinhold BB, Petráková E, Yeh HJC, Ashwell G, Drgonová J, Kapteyn JC, Klis FM, Cabib E (1997) Architecture of the yeast cell wall: β-1,6-glucan interconnects mannoprotein, β-1,3-glucan, and chitin. J Biol Chem 272:17762–17788PubMedCrossRefGoogle Scholar
  102. Kondoh O, Tachibana Y, Ohya Y, Arisawa M, Watanabe T (1997) Cloning of the RHO1 gene from Candida albicans and its regulation of beta-1,3-glucan synthesis. J Bacteriol 179:7734–7741PubMedGoogle Scholar
  103. Kopecka M, Gabriel M (1992) The influence of Congo Red on the cell wall and (1–3)-beta-d-glucan microfibril biogenesis on Saccharomyces cerevisiae. Arch Microbiol 158:115–126PubMedCrossRefGoogle Scholar
  104. Koyama M, Helbert W, Tomoya I, Sugiyama J, Henrissat B (1997) Parallel-up structure evidences the molecular directionality during biosynthesis of bacterial cellulose. Proc Natl Acad Sci USA 94:9091–9095PubMedCrossRefGoogle Scholar
  105. Kreger DR (1954) Observations on cell walls of yeasts and some other fungi by X-ray diffraction and solubility tests. Biochim Biophys Acta 13:1–9PubMedCrossRefGoogle Scholar
  106. Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (1990) Biochemistry of cell walls and membranes in fungi. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  107. Kurtz MB, Douglas CM (1997) Lipopeptide inhibitors of fungal glucan synthase. J Med Vet Mycol 35:79–86PubMedCrossRefGoogle Scholar
  108. Kurtz MB, Heath IB, Marrinan J, Dreikorn S, Onishi J, Douglas C (1994) Morphological effects of lipopeptides against Aspergillus fumigatus correlate with activities against (l,3)-β-d-glucan synthase. Antimicrob Agents Chemother 38:1480–1489PubMedCrossRefGoogle Scholar
  109. Leal J-A, Jiménez-Barbero J, Gómez-Miranda B, Prieto A, Domenech J, Bernabé M (1996) Structural investigation of a cell-wall galactomannan from Neurospora crassa and N. sitophila. Carbohydr Res 283:215–222PubMedCrossRefGoogle Scholar
  110. Leal-Morales CA, Bracker CE, Bartnicki-Garcia S (1994) Subcellular localization, abundance and stability of chitin synthetases 1 and 2 from Saccharomyces cerevisiae. Microbiology 140:2207–2216PubMedCrossRefGoogle Scholar
  111. Lora JM, de la Cruz J, Benitez T, Llobell A, Pintor-Toro JA (1994) A putative catabolite-repressed cell wall protein from the mycoparasitic fungus Trichoderma harzianum. Mol Gen Genet 242:461–466PubMedCrossRefGoogle Scholar
  112. Lu CF, Kurjan J, Lipke PN (1994) A pathway for cell wall anchorage of Saccharomyces cerevisiaeα-agglutinin. Mol Cell Biol 9:4825–4833Google Scholar
  113. Lussier M, White AM, Sheraton J, di Paolo T, Treadwell J, Southard SB, Horenstein CI, Chen-Weiner J, Ram AF, Kapteyn JC, Roemer TW, Vo DH, Bondoc DC, Hall J, Zhong WW, Sdicu AM, Davies J, Klis FM, Robbins PW, Bussey H (1997) Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147: 435–450PubMedGoogle Scholar
  114. Lussier M, Sdicu AM, Shahinian S, Bussey H (1998) The Candida albicans KRE9 gene is required for cell wall beta-1,6-glucan synthesis and is essential for growth on glucose. Proc Natl Acad Sci USA 95: 9825–9830PubMedCrossRefGoogle Scholar
  115. Maeda H, Ishida N (1967) Specificity of binding of hexopyranosyl polysaccharides with fluorescent brightener. J Biochem (Tokyo) 62:276–278Google Scholar
  116. Manners DJ, Masson AJ, Patterson JC (1973a) The structure of a β-(1–3)-d-glucan from yeast cell walls. Biochem J 135:19–30PubMedGoogle Scholar
  117. Manners DJ, Masson AJ, Patterson JC, Bjorndal H, Lindberg B (1973b) The structure of a β-(1–6)-d-glucan from yeast cell walls. Biochem J 135:31–36PubMedGoogle Scholar
  118. Marchessault RH, Deslandes Y (1979) Fine structure of (1–3)-β-glucans: curdlan and paramylon. Carbohydr Res 75:231–242CrossRefGoogle Scholar
  119. Martin F, Laurent P, de Carvalho D, Voiblet C, Balestrini R, Bonfante P,Tagu D (1999) Cell wall proteins of the ectomycorrhizal basidiomycete Pisolithus tinctorius: identification, function and expression in symbiosis. Fungal Genet Biol 27:161–174PubMedCrossRefGoogle Scholar
  120. Martinez FA, Schwencke J (1988) Chitin synthetase activity is bound to chitosomes and to the plasma membrane in protoplasts of Saccharomyces cerevisiae. Biochim Biophys Acta 946:328–336CrossRefGoogle Scholar
  121. Mazur P, Baginsky W (1996) In vitro activity of 1,3-beta-d-glucan synthase requires the GTP-binding protein Rhol. J Biol Chem 271:14604–14609PubMedCrossRefGoogle Scholar
  122. McCreath KJ, Specht CA, Robbins PW (1995) Molecular cloning and characterization of chitinase genes from Candida albicans. Proc Natl Acad Sci USA 92: 2544–2548PubMedCrossRefGoogle Scholar
  123. Mio T, Yabe T, Sudoh M, Satoh Y, Nakajima T, Arisawa M, Yamada-Okabe H (1996) Role of three chitin synthase genes in the growth of Candida albicans. J Bacteriol 178:2416–2419PubMedGoogle Scholar
  124. Mio T, Adachi-Shimizu M, Tachibana Y, Tabuchi H, Inoue S, Yabe T, Yamada-Okabe T, Arisawa M, Watanabe T, Yamada-Okabe H (1997) Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/ FKS1 and its involvement in β-1,3-glucan synthesis. J Bacteriol 179:4096–4105PubMedGoogle Scholar
  125. Mirelman D, Galun E, Sharon N, Loan R (1975) Inhibition of fungal growth by wheat germ agglutinin. Nature 256:414–416PubMedCrossRefGoogle Scholar
  126. Miyata M, Kanbe T, Tanaka K (1985) Morphological alterations of the fission yeast Schizosaccharomyces pombe in the presence of aculeacin A: spherical wall formation. J Gen Microbiol 131:611–621Google Scholar
  127. Mol PC, Wessels JGH (1987) Linkages between glucosaminoglycan and glucan determine alkali-insolubility of the glucan in walls of S cerevisiae. FEMS Microbiol Lett 41:95–99CrossRefGoogle Scholar
  128. Molloy C, Shepherd MG, Sullivan PA (1989) Identification of envelope proteins of Candida albicans by vectorial iodination. Microbios 57:73–84PubMedGoogle Scholar
  129. Montijn RC, Van Wolven P, De Hoog S, Klis FM (1997) Beta-glucosylated proteins in the cell wall of the black yeast Exophiala (Wangiella) dermatitidis. Microbiology 143:1673–1680PubMedCrossRefGoogle Scholar
  130. Montijn RC, Vink E, Müller WH, Verkley AJ, Van Den Ende H, Henrissat B, Klis FM (1999) Localization of the synthesis of β1,6-glucan in Saccharomyces cerevisiae. J Bacteriol 181:7414–7420PubMedGoogle Scholar
  131. Morawetz R, Lendenfeld T, Mischak H, Muhlbauer M, Gruber F, Goodnight J, de Graaff LH, Visser J, Mushinski JF, Kubicek CP (1996) Cloning and characterisation of genes (pkc1 and pkcA) encoding protein kinase C homologues from Trichoderma reesei and Aspergillus niger. Mol Gen Genet 250:17–28PubMedGoogle Scholar
  132. Mouyna I, Hartland RP, Fontaine T, Diaquin M, Simenel C, Delepierre M, Henrissat B, Latge JP (1998) A 1,3-beta-glucanosyltransferase isolated from the cell wall of Aspergillus fumigatus is a homologue of the yeast Bgl2p. Microbiology 144:3171–3180PubMedCrossRefGoogle Scholar
  133. Mouyna I, Vai T, Fontaine M, Monod M, Fonzi WA, Diaquin M, Popolo L, Henrissat B, Hartland RP, Largé JP (1999) The protein encoded by GAS1 of Saccharomyces cerevisiae displays the same enzymatic activity as Gel1p of Aspergillus fumigatus and corresponds to a β(1–3)glucanosyltransferase. Curr Genet 35:440Google Scholar
  134. Mühlschlegel FA, Fonzi WA (1997) PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol Cell Biol 17:5960–5967PubMedGoogle Scholar
  135. Mrsa V, Seidl M, Gentzsch M, Tanner W (1997) Specific labeling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of S. cerevisiae. Yeast 13:1145–1149PubMedCrossRefGoogle Scholar
  136. Nagahashi S, Lussier M, Bussey H (1998) Isolation of Candida glabrata homologs of the Saccharomyces cerevisiae KRE9 and KNH1 genes and their involvement in cell wall beta-l,6-glucan synthesis. J Bacteriol 180:5020–5029PubMedGoogle Scholar
  137. Nakajima T, Yoshida M, Nakamura M, Hiura N, Matsuda K (1984) Structure of the cell wall proteogalactomannan from Neurospora crassa. II. Structural analysis of the polysaccharide part. J Biochem (Tokyo) 96: 1013–1020Google Scholar
  138. Nakazawa T, Horiuchi H, Ohta A, Takagi M (1998) Isolation and characterization of EPD1, an essential gene for pseudohyphal growth of a dimorphic yeast, Candida maltosa. J Bacteriol 180:2079–2086PubMedGoogle Scholar
  139. Navarro-Garcia F, Alonso-Monge R, Rico H, Pla J, Sen-tandreu R, Nombela C (1998) A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 144:411–424PubMedCrossRefGoogle Scholar
  140. Nguyen TH, Fleet GH, Rogers PL (1998) Composition of the cell walls of several yeast species. Appl Microbiol Biotechnol 50:206–212PubMedCrossRefGoogle Scholar
  141. Orlean P (1997) Biogenesis of yeast wall and surface components. In: Pringle JR, Broach JR, Jones EW (eds) The Molecular and Cellular Biology of the Yeast Saccharomyces, vol 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 229–362Google Scholar
  142. Orlean PAB, Krag SS (eds) (1999) Glycans of the secretory pathway in yeast. Biochim Biophys Acta 1426, no 2, Special IssueGoogle Scholar
  143. Osmond BC, Specht CA, Robbins PW (1999) Chitin synthase. III. Synthetic lethal mutants and “stress related” chitin synthesis that bypasses the CSD3/CHS6 localization pathway. Proc Natl Acad Sci USA 96:11206–11210PubMedCrossRefGoogle Scholar
  144. Park IC, Horiuchi H, Hwang CW, Yeh WH, Ohta A, Ryu JC, Takagi M (1999) Isolation of csm1 encoding a class V chitin synthase with a myosin motor-like domain from the rice blast fungus, Pyricularia oryzae. FEMS Microbiol Lett 170:131–139PubMedCrossRefGoogle Scholar
  145. Peberdy JF (1990) Fungal cell walls — a review. In: Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (eds) Biochemistry of cell walls and membranes in fungi. Springer, Berlin Heidelberg New York, pp 5–30CrossRefGoogle Scholar
  146. Polacheck I, Rosenberger RF (1977) Aspergillus nidulans mutant lacking alpha-(1,3)-glucan, melanin, and cleis-tothecia. J Bacteriol 132:650–656PubMedGoogle Scholar
  147. Popolo L, Vai M (1999) The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim Biophys Acta 1426:385–400PubMedCrossRefGoogle Scholar
  148. Popolo L, Gilardelli D, Bonfante P, Vai M (1997) Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1 ... mutant of Saccharomyces cerevisiae. J Bacteriol 179:463–469PubMedGoogle Scholar
  149. Qadota H, Python CP, Inoue SB, Arisawa M, Anraku Y, Zheng Y, Watanabe T, Levin DE, Ohya Y (1996) Identification of yeast Rholp GTPase as a regulatory subunit of 1,3-beta-glucan synthase. Science 272: 279–281PubMedCrossRefGoogle Scholar
  150. Ram AF, Wolters A, Ten Hoopen R, Klis FM (1994) A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white. Yeast 10:1019–1030PubMedCrossRefGoogle Scholar
  151. Ram AFJ, Kapteyn JC, Montijn RC, Caro LH, Douwes JE, Baginsky W, Mazur P, Van den Ende H, Klis FM (1998) Loss of the plasma membrane bound protein Gas1p in Saccharomyces cerevisiae results in the release of β1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J Bacteriol 180:1418–1424PubMedGoogle Scholar
  152. Rico H, Herrero E, Miragall F, Sentandreu R (1991) An electron microscopy study of wall expansion during Candida albicans yeast and mycelial growth using concanavalin A-ferritin labelling of mannoproteins. Arch Microbiol 156:111–114PubMedCrossRefGoogle Scholar
  153. Roemer T, Bussey H (1995) Yeast Kre1p is a cell surface O-glycoprotein. Mol Gen Genet 249:209–216PubMedCrossRefGoogle Scholar
  154. Roncero C, Duran A (1985) Effect of calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol 163:1180–1185PubMedGoogle Scholar
  155. Roncero C, Valdivieso MH, Ribas JC, Duran A (1988) Isolation and characterization of Saccharomyces cerevisiae mutants resistant to calcofluor white. J Bacteriol 170:1950–1954PubMedGoogle Scholar
  156. Ruiz-Herrera J (1992) Fungal cell wall. Structure, synthesis, and assembly. CRC Press, Boca RatonGoogle Scholar
  157. Russo P, Kalkkinen N, Sareneva H, Paakkola J, Makarow M (1992) A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc Natl Acad Sci USA 89:3671–3675PubMedCrossRefGoogle Scholar
  158. San-Blas G, San-Blas F (1977) Paracoccidioides brasiliensis :cell wall structure and virulence. A review. Mycopathology 62:77–86CrossRefGoogle Scholar
  159. Saporito-Irwin SM, Birse CE, Sypherd PS, Fonzi WA (1995) PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol Cell Biol 15:601–613PubMedGoogle Scholar
  160. Schekman R, Brawley V (1979) Localized deposition of chitin on the yeast cell surface in response to mating pheromone. Proc Natl Acad Sci USA 76:645–649PubMedCrossRefGoogle Scholar
  161. Schoffelmeer EAM (1999) Biochemical aspects of the cell wall of Fusarium oxysporum. PhD thesis, University of Amsterdam, The NetherlandsGoogle Scholar
  162. Schoffelmeer EAM, Klis FM, Sietsma JGH, Cornelissen BJC (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27:275–282PubMedCrossRefGoogle Scholar
  163. Schreuder MP, Mooren ATA,Toschka HY, Verrips CT, Klis FM (1996) Immobilizing proteins on the surface of yeast cells. Trends Biotechnol 14:115–120PubMedCrossRefGoogle Scholar
  164. Sentandreu R, Mormeneo S, Ruiz-Herrera J (1994) Biogenesis of the fungal cell wall. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol 1. Springer, Berlin Heidelberg New York, pp 111–124Google Scholar
  165. Shaw JA, Mol PC, Bowers B, Silverman SJ, Valdivieso MH, Duran A, Cabib EJ (1991) The function of chitin synthase-2 and synthase-3 in the Saccharomycescerevisiae cell cycle. J Cell Biol 114:111–123PubMedCrossRefGoogle Scholar
  166. Shematek EM, Braatz JA, Cabib E (1980) Biosynthesis of the yeast cell wall. I. Preparation and properties of β-1,3-gluean synthetase. J Biol Chem 255:888–894PubMedGoogle Scholar
  167. Shepherd MG (1987) Cell envelope of Candida albicans. Crit Rev Microbiol 15:7–25PubMedCrossRefGoogle Scholar
  168. Sietsma JH, Wessels JG (1977) Chemical analysis of the hyphal wall of Schizophyllum commune. Biochim Biophys Acta 496:225–239PubMedCrossRefGoogle Scholar
  169. Sietsma JH, Wessels JGH (1981) Solubility of (1→3)-beta-d/(126)-beta-d-glucan in fungal walls: importance of presumed linkage between glucan and chitin. J Gen Microbiol 125:209–212PubMedGoogle Scholar
  170. Sietsma JH, Wessels JGH (1990) The occurrence of glucosaminoglycan in the wall of Schizosaccharomyces pombe. J Gen Microbiol 136:2261–2265PubMedGoogle Scholar
  171. Sietsma JH, Wessels JGH (1994) Apical wall biogenesis. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol 1. Springer, Berlin Heidelberg New York, pp 125–141Google Scholar
  172. Sietsma JH, Beth-Din A, Ziv V, Sjollema KA, Yarden O (1996) The localization of chitin synthase in membranous vesicles (chitosomes) in Neurospora crassa. Microbiology 142:1591–1596PubMedCrossRefGoogle Scholar
  173. Smits G, Kapteyn JC, Van Den Ende H, Klis FM (1999) Cell wall dynamics in yeast. Curr Opin Microbiol 2:348–352PubMedCrossRefGoogle Scholar
  174. Specht CA, Liu Y, Robbins PW, Bulawa CE, Iartchouk N, Winter KR, Riggle PJ, Rhodes JC, Dodge CL, Culp DW, Borgia PT (1996) The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis. Fungal Genet Biol 20:153–167PubMedCrossRefGoogle Scholar
  175. Staab JF, Sundstrom P (1998) Genetic organization and sequence analysis of the hypha-specific cell wall protein gene HWP1 of Candida albicans. Yeast 14: 681–686PubMedCrossRefGoogle Scholar
  176. Staab JF, Ferrer CA, Sundstrom P (1996) Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces on Candida albicans. J Biol Chem 271:6298–6305PubMedCrossRefGoogle Scholar
  177. Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 1535–1538PubMedCrossRefGoogle Scholar
  178. Staebell M, Soll DR (1985) Temporal and spatial differences in cell wall expansion during bud and mycelium formation in Candida albicans. J Gen Microbiol 131:1467–1480PubMedGoogle Scholar
  179. St Leger RJ, Staples RC, Roberts DW (1992) Cloning and regulatory analysis of starvation-stress gene, ssgA, encoding a hydrophobin like protein from the entomopathogenic fungus Metarizium anisopliae. Gene 120:119–124CrossRefGoogle Scholar
  180. Strahl-Bolsinger S, Gentzsch M, Tanner W (1999) Protein O-mannosylation. Biochim Biophys Acta 1426: 297–308PubMedCrossRefGoogle Scholar
  181. Stringer MA, Dean RA, Sewall TC, Timberlake WE (1991) Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Genes Dev 5:1161–1171PubMedCrossRefGoogle Scholar
  182. Surarit R, Gopal PK, Shepherd MG (1988) Evidence for a glycosidic linkage between chitin and glucan in the cell wall of Candida albicans. J Gen Microbiol 134:1723–1730PubMedGoogle Scholar
  183. Szaniszlo PJ, Kang MS, Cabib E (1985) Stimulation of beta(l-3)glucan synthetase of various fungi by nucleoside triphosphates: generalized regulatory mechanism for cell wall biosynthesis. J Bacteriol 161: 1188–1194PubMedGoogle Scholar
  184. Talbot NJ (1997) Fungal biology: growing into the air. Curr Biol 7:R78–R81PubMedCrossRefGoogle Scholar
  185. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grísea. Plant Cell 5:1575–1590PubMedGoogle Scholar
  186. Tanaka H,Watanabe T (1995) Glucanases and chitinases of Bacillus circulans WL-12. J Ind Microbiol 14:478–483PubMedCrossRefGoogle Scholar
  187. Tanaka K, Nambu H, Katoh Y, Kai M, Hidaka Y (1999) Molecular cloning of homologs of RAS and RHO1 genes from Cryptococcus neoformans. Yeast 15: 1133–1139PubMedCrossRefGoogle Scholar
  188. Thompson JR, Douglas CM, Li W, Jue CK, Pramanik B, Yuan X, Rude TH, Toff aletti DL, Perfect JR, Kurtz M (1999) A glucan synthase FKS1 homolog in Cryptococcus neoformans is single copy and encodes an essential function. J Bacteriol 181:444–453PubMedGoogle Scholar
  189. Toda T, Dhut S, Superti-Furga G, Gotoh Y, Nishida E, Sugiura R, Kuno T (1996) The fission yeast pmk1+ gene encodes a novel mitogen-activated protein kinase homolog which regulates cell integrity and functions coordinately with the protein kinase C pathway. Mol Cell Biol 16:6752–6764PubMedGoogle Scholar
  190. Toh-e A, Yasunaga S, Nisogi H, Tanaka K, Oguchi T, Matsui Y (1993) Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock. Yeast 9:481–494CrossRefGoogle Scholar
  191. Trinci APJ, Collinge AJ (1975) Hyphal wall growth in Neurospora crassa and Geotrichum candidum. J Gen Microbiol 91:355–361PubMedGoogle Scholar
  192. Trinci APJ, Wiebe MG, Robson GD (1994) The mycelium as an integrated entity. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol 1. Springer, Berlin Heidelberg New York, pp 175–193Google Scholar
  193. Valdivieso MH, Mol PC, Shaw JA, Cabib E, Duran A (1991) CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J Cell Biol 114:101–109PubMedCrossRefGoogle Scholar
  194. Valentin E, Herrero W, Pastor JFI, Sentandreu R (1984) Solubilization and analysis of mannoprotein molecules from the cell wall of Saccharomyces cerevisiae. J Gen Microbiol 130:1419–1428Google Scholar
  195. Van der Valk P, Marchant R, Wessels JGH (1977) Ultra-structural localization of polysaccharides in the wall and septum of the basidiomycete Schizophyllum commune. Exp My col 1:69–82CrossRefGoogle Scholar
  196. Vermeulen CA, Wessels JGH (1986) Chitin biosynthesis by a fungal membrane preparation. Evidence for a transient non-crystalline state of chitin. Eur J Biochem 158:411–415PubMedCrossRefGoogle Scholar
  197. Villa TG, Notario V, Villanueva JR (1980) Chemical and enzymic analysis of Pichia polymorpha cell walls. Can J Microbiol 26:169–174PubMedCrossRefGoogle Scholar
  198. Von Sengbusch P, Hechler J, Müller U (1983) Molecular architecture of fungal cell walls. An approach by use of fluorescent markers. Eur J Cell Biol 30:305–312Google Scholar
  199. Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Annu Rev Phytopathol 32:413–437CrossRefGoogle Scholar
  200. Wessels JGH (1996) Fungal hydrophobins: proteins that function at an interface. Trends Plant Sciences 1:9–15CrossRefGoogle Scholar
  201. Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45PubMedCrossRefGoogle Scholar
  202. Wessels JGH, Sietsma JH (1981) Fungal cell walls: a survey. In: Tanner W, Loewus FA (eds) Encyclopedia of plant physiology, vol 13B. Plant carbohydrates II. Extracellular carbohydrates. Springer, Berlin Heidelberg New York, pp 352–394CrossRefGoogle Scholar
  203. Williamson G, Belshaw NJ, Williamson MP (1992) O-Glycosylation in Aspergillus glucoamylase. Confirmation and role in binding. Biochem J 282:423–428PubMedGoogle Scholar
  204. Wood PJ (1980) Specificity in the interaction of direct dyes with polysaccharides. Carbohydr Res 85:271–287CrossRefGoogle Scholar
  205. Wösten HAB, De Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a rodlet layer. Plant Cell 5:1567–1574PubMedGoogle Scholar
  206. Wösten HAB, Asgeirsdottir SA, Krook JH, Drenth JHH, Wessels JGH (1994) The Sc3p hydrophobin self-assembles at the surface of aerial hyphae as a protein membrane constituting the hydrophobic rodlet layer. Eur J Cell Biol 63:122–129PubMedGoogle Scholar
  207. Wösten HAB, Richter M, Willey JM (1999) Structural proteins involved in emergence of microbial aerial hyphae. Fungal Genet Biol 27:153–160PubMedCrossRefGoogle Scholar
  208. Xoconostle-Cazares B, Specht CA, Robbins PW, Liu Y, Leon C, Ruiz-Herrera J (1997) Umchs5, a gene coding for a class IV chitin synthase in Ustilago maydis. Fungal Genet Biol 22:199–208PubMedCrossRefGoogle Scholar
  209. Yu L, Goldman R, Sullivan P, Walker GF, Fesik SW (1993) Heteronuclear NMR studies of 13C-labeled yeast cell wall beta-glucan oligosaccharides. J Biomol NMR 3: 429–441PubMedCrossRefGoogle Scholar
  210. Zhu Y, Yang C, Magee DM, Cox RA (1996) Coccidioides immitis antigen 2: analysis of gene and protein. Gene 181:121–125PubMedCrossRefGoogle Scholar
  211. Ziman M, Chuang JS, Schekman RW (1996) Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol Biol Cell 7:1909–1919PubMedGoogle Scholar
  212. Zlotnik H, Fernandez MP, Bowers B, Cabib E (1984) Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J Bacteriol 159:1018–1026PubMedGoogle Scholar
  213. Zonneveld BJ (1972) Morphogenesis in Aspergillus nidulans. The significance of α-1,3-glucan of the cell wall and α-1,3-glucanase for cleistothecium development. Biochim Biophys Acta 273:174–187PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • Hans De Nobel
    • 1
  • J. Hans Sietsma
    • 2
  • Herman Van Den Ende
    • 1
  • Frans M. Klis
    • 1
  1. 1.Swammerdam Institute for Life SciencesUniversity of AmsterdamAmsterdamThe Netherlands
  2. 2.Molecular Plant Biology Laboratory, Groningen Biomolecular Sciences and Biotechnology Institute (GBB)University of GroningenHarenThe Netherlands

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