Cell Biology of Fungal Infection of Plants

  • Adrienne R. Hardham
Part of the The Mycota book series (MYCOTA, volume 8)


Plants are, in general, resistant to the attempts of potential fungal pathogens to infect them. Those fungi that do succeed in establishing infection and disease, however, cause widespread environmental damage and economic losses. In order to establish infection, fungal pathogens must overcome highly effective, constitutive physical and chemical barriers to pathogen ingress. They must avoid inducing additional host defenses, and they must be able to deploy mechanisms for obtaining from the plant the nutrients they need for growth and reproduction. In order to meet all these requirements, successful fungal pathogens employ a range of different infection strategies. The details of these strategies may be specific to a particular fungal species, they may differ according to the nature of the plant surface, and they may depend within a single species on the type of spore initiating the infection process.


Germ Tube Rust Fungus Appressorium Formation Apical Vesicle Intracellular Hypha 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Adachi K, Hamer JE (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grísea. Plant Cell 10: 1361–1373PubMedGoogle Scholar
  2. Aist JR, Bushnell WR (1991) Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance. In: Cole GT Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 321–345Google Scholar
  3. Allan RH, Thorpe CJ, Deacon JW (1992) Differential tropism to living and dead cereal root hairs by the biocontrol fungus Idriella bolleyi. Physiol Mol Plant Pathol 41:217–226CrossRefGoogle Scholar
  4. Allaway WG, Ashford AE, Heath IB, Hardham AR (1998) Vacuolar reticulum in oomycete hyphal tips: an additional component of the Ca2+ regulatory system? Fungal Genet Biol 22:209–220CrossRefGoogle Scholar
  5. Apel-Birkhold PC, Walton JD (1996) Cloning, disruption, and expression of two endo-β1,4-xylanase genes, XYL2 and XYL3, from Cochliobolus carbonum. Appl Environ Microbiol 62:4129–4135PubMedGoogle Scholar
  6. Apel PC, Panaccione DG, Holden FR, Walton JD (1993) Cloning and targeted gene disruption of XYL1, a β1,4-xylanase gene from the maize pathogen Cochliobolus carbonum. Mol Plant Microbe Interact 6:467–473PubMedCrossRefGoogle Scholar
  7. Armentrout VN, Downer AJ, Grasmick DL, Weinhold AR (1987) Factors affecting infection cushion development by Rhizoctonia solani on cotton. Phytopathology 77:623–630CrossRefGoogle Scholar
  8. Ayscough KR, Stryker J, Pokala N, Sanders M, Crews P, Drubin DG (1997) High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 137:399–416PubMedCrossRefGoogle Scholar
  9. Bachewich C, Heath IB (1998) Radial F-actin arrays precede new hypha formation in Saprolegnia: implications for establishing polar growth and regulating tip morphogenesis. J Cell Sci 111:2005–2016PubMedGoogle Scholar
  10. Bachewich C, Heath IB (1999) Cytoplasmic migrations and vacuolation are associated with growth recovery in hyphae of Saprolegnia, and are dependent on the cytoskeleton. Mycol Res 103:849–858CrossRefGoogle Scholar
  11. Baka ZA, Larous L, Lösel DM (1995) Distribution of ATPase activity at the host-pathogen interfaces of rust infections. Physiol Mol Plant Pathol 47:67–82CrossRefGoogle Scholar
  12. Barja F, Chappuis M-L, Tunan G (1993) Differential effects of anticytoskeletal compounds on the localization and chemical patterns of actin in germinating conidia of Neurospora crassa. FEMS Microbiol Lett 107:261–266PubMedCrossRefGoogle Scholar
  13. Bartnicki-Garcia S (1973) Fundamental aspects of hyphal morphogenesis. In: Ashworth JM, Smith JE (eds) Microbial differentiation. Cambridge Univ Press, Cambridge, pp 245–267Google Scholar
  14. Bartnicki-Garcia S (1996) The hypha: unifying thread of the fungal kingdom. In: Sutton BC (ed) A century of mycology. Cambridge Univ Press, Cambridge, pp 105–133Google Scholar
  15. Bartnicki-Garcia S, Sing VO (1987) Adhesion of zoospores of Phytophthora to solid surfaces. In: Fuller MS, Jaworski A (eds) Zoosporic fungi in teaching & research. Southeastern Publishing Corporation, Athens, GA, pp 279–283Google Scholar
  16. Bartnicki-Garcia S, Hergert F, Gierz G (1989) Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153:46–57CrossRefGoogle Scholar
  17. Bartnicki-Garcia S, Hergert F, Gierz G (1990) A novel computer model for generating cell shape: application to fungal morphogenesis. 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 43–60CrossRefGoogle Scholar
  18. Bechinger C, Giebel K-F, Schnell M, Leiderer P, Deising HB, Bastmeyer M (1999) Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285:1896–1899PubMedCrossRefGoogle Scholar
  19. Beckerman JL, Ebbole DJ (1996) MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Mol Plant Microbe Interact 9:450–456PubMedCrossRefGoogle Scholar
  20. Bimpong CE, Hickman CJ (1975) Ultrastructural and cytochemical studies of zoospores, cysts, and germinating cysts of Phytophthora palmivora. Can J Bot 53:1310–1327CrossRefGoogle Scholar
  21. Bourett TM, Howard RJ (1990) In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Can J Bot 68:329–342CrossRefGoogle Scholar
  22. Bourett TM, Howard RJ (1991) Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163:199–202CrossRefGoogle Scholar
  23. Bourett TM, Howard RJ (1992) Actin in penetration pegs of the fungal rice blast pathogen, Magnaporthe grisea. Protoplasma 168:20–26CrossRefGoogle Scholar
  24. Bourett T, Hoch HC, Staples RC (1987) Association of the microtubule cytoskeleton with the thigmotropic signal for appressorium formation in Uromyces. Mycologia 79:540–545CrossRefGoogle Scholar
  25. Bourett TM, Czymmek KJ, Howard RJ (1998) An improved method for affinity probe localization in whole cells of filamentous fungi. Fungal Genet Biol 24:3–13PubMedCrossRefGoogle Scholar
  26. Bourne HR (1997) How receptors talk to trimeric G proteins. Curr Opin Cell Biol 9:134–42PubMedCrossRefGoogle Scholar
  27. Bowen JK, Templeton MD, Sharrock KR, Crowhurst RN, Rikkerink EHA (1995) Gene inactivation in the plant pathogen Glomerella cingulata: three strategies for the disruption of the pectin lyase gene pnl A. Mol Gen Genet 246:196–205PubMedCrossRefGoogle Scholar
  28. Bracker CE, Ruiz-Herrera J, Bartnicki-Garcia S (1976) Structure and transformation of chitin synthetase particles (chitosomes) during microfibril synthesis in vitro. Proc Natl Acad Sci USA 73:4570–4574PubMedCrossRefGoogle Scholar
  29. Brambl R, Dunkle LD, Van Etten JL (1978) Nucleic acid and protein synthesis during fungal spore germination. In: Smith JE, Berry DR (eds) The filamentous fungi. Arnold, London, pp 94–118Google Scholar
  30. Braun EJ, Howard RJ (1994a) Adhesion of fungal spores and germlings to host plant surfaces. Protoplasma 181:202–212CrossRefGoogle Scholar
  31. Braun EJ, Howard RJ (1994b) Adhesion of Cochliobolus heterostrophus conidia and germlings to leaves and artificial surfaces. Exp Mycol 18:211–220CrossRefGoogle Scholar
  32. Bullock S, Ashford AE, Willets HJ (1980) The structure and histochemistry of sclerotia of Sclerotinia minor Jagger II. Histochemistry of extracellular substances and cytoplasmic reserves. Protoplasma 104:333–351CrossRefGoogle Scholar
  33. Bullock S, Willets HJ, Ashford AE (1983) The structure and histochemistry of sclerotia of Sclerotinia minor Jagger III. Changes in ultrastructure and loss of reserve materials during carpogenic germination. Protoplasma 117:214–225CrossRefGoogle Scholar
  34. Callow JA, Green JR (1996) The plant plasma membrane in fungal disease. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. Bios Scientific Publishers, Oxford, pp 543–562Google Scholar
  35. Callow JA, Mackie A, Roberts AM, Green JR (1992) Evidence for molecular differentiation in powdery mildew haustoria through the use of monoclonal antibodies. Symbiosis 14:237–246Google Scholar
  36. Carver TLW, Thomas BJ, Ingerson-Morris SM (1995) The surface of Erysiphe graminis and the production of extracellular material at the fungus-host interface during germling and colony development. Can J Bot 73:272–287CrossRefGoogle Scholar
  37. Chard JM, Gay JL (1984) Characterization of the parasitic interface between Erysiphe pisi and Pisum sativum using fluorescent probes. Physiol Plant Pathol 25: 259–276CrossRefGoogle Scholar
  38. Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973–1983PubMedGoogle Scholar
  39. Chong J, Harder DE, Rohringer R (1981) Ontogeny of mono- and dikaryotic rust haustoria: cytochemical and ultrastructural studies. Phytopathology 71:975–983CrossRefGoogle Scholar
  40. Chumley FG, Valent B (1990) Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol Plant Microbe Interact 3:135–143CrossRefGoogle Scholar
  41. Clark MC, Melansson DL, Page OT (1978) Purine metabolism and differentiatial inhibition of spore germination in Phytophthora infestans. Can J Microbiol 24: 1032–1038PubMedCrossRefGoogle Scholar
  42. Clay RP, Bergmann CW, Fuller MS (1997) Isolation and characterization of an endopolygalacturonase from Cochliobolus sativus and a cytological study of fungal penetration of barley. Phytopathology 87:1148–1159PubMedCrossRefGoogle Scholar
  43. Clement JA, Porter R, Butt TM, Beckett A (1994) The role of hydrophobicity in attachment of urediniospores and sporelings of Uromyces viciae-fabae. Mycol Res 98:1217–1228CrossRefGoogle Scholar
  44. Clement JA, Porter R, Butt TM, Beckett A (1997) Characteristics of adhesion pads formed during imbibition and germination of urediniospores of Uromyces viciae-fabae on host and synthetic surfaces. Mycol Res 101:1445–1458CrossRefGoogle Scholar
  45. Cole L, Orlovich DA, Ashford AE (1998) Structure, function, and motility of vacuoles in filamentous fungi. Fungal Genet Biol 24:86–100PubMedCrossRefGoogle Scholar
  46. Coleman JOD, Hiscock SJ, Dewey FM (1993) Monoclonal antibodies to purified cutinase from Fusarium solarti f. sp. pisi. Physiol Mol Plant Pathol 43:391–401CrossRefGoogle Scholar
  47. Collins TJ, Read ND (1997) Appressorium induction by topographical signals in six cereal rusts. Physiol Mol Plant Pathol 51:169–179CrossRefGoogle Scholar
  48. Cope M, Webb MC, O’Gara ET, Philip BA, Hardham AR (1996) Immunocytochemical comparison of peripheral vesicles in zoospores of Phytophthora and Pythium species. Mycologia 88:523–532CrossRefGoogle Scholar
  49. Corrêa A Jr, Hoch HC (1995) Identification of thigmore-sponsive loci for cell differentiation in Uromyces germlings. Protoplasma 186:34–40CrossRefGoogle Scholar
  50. Corrêa A Jr, Staples RC, Hoch HC (1996) Inhibition of thig-mostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194:91–102CrossRefGoogle Scholar
  51. Czymmek KJ, Bourett TM, Howard RJ (1996) Immunolo-calization of tubulin and actin in thick-sectioned fungal hyphae after freeze-substitution fixation and methacrylate de-embedment. J Microsc 181:153–161CrossRefGoogle Scholar
  52. Deacon JW (1997) Modern mycology. Blackwell Science, OxfordGoogle Scholar
  53. Dean RA (1997) Signal pathways and appressorium morphogenesis. Annu Rev Phytopathol 35:211–234PubMedCrossRefGoogle Scholar
  54. Dearnaley JDW, Maleszka J, Hardham AR (1996) Synthesis of zoospore peripheral vesicles during sporulation of Phytophthora cinnamomi. Mycol Res 100:39–48CrossRefGoogle Scholar
  55. Deising H, Mendgen K (1992) Developmental control of enzyme production and cell wall modification in rust fungi, and defence reactions of the host plant. In: Stahl, U,Tudzynski, P (eds) Molecular biology of filamentous fungi. VCH, Weinheim, pp 27–44Google Scholar
  56. Deising H, Nicholson RL, Haug M, Howard RJ, Mendgen K (1992) Adhesion pad formation and the involvement of cutinase and esterases in the attachment of urediospores to the host cuticle. Plant Cell 4:1101–1111PubMedGoogle Scholar
  57. Deising H, Rauscher M, Haug M, Heiler S (1995a) Differentiation and cell wall degrading enzymes in the oblig-ately biotrophic rust fungus Uromyces viciae-fabae. Can J Bot 73 [Suppl 1]:S624–S631CrossRefGoogle Scholar
  58. Deising H, Frittrang AK, Kunz S, Mendgen K (1995b) Regulation of pectin methylesterase and poly-galacturonate lyase activity during differentiation of infection structures in Uromyces viciae-fabae. Microbiology 141:561–571CrossRefGoogle Scholar
  59. Deising H, Heiler S, Rauscher M, Xu H, Mendgen K (1996) Cellular aspects of rust infection structure differentiation. In: Nicole M, Gianinazzi-Pearson V (eds) Histology, ultrastructure and molecular cytology of plant-microorganism interactions. Kluwer, Dordrecht, pp 135–156CrossRefGoogle Scholar
  60. deJong JC, McCormack BJ, Smirnoff N, Talbot NJ (1997) Glycerol generates turgor in rice blast. Nature 389: 244–245CrossRefGoogle Scholar
  61. DeZwaan TM, Carroll AM, Valent B, Sweigard JA (1999) Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11:2013–2030PubMedGoogle Scholar
  62. Dickinson S (1979) Growth of Erysiphe graminis on artificial membranes. Physiol Plant Pathol 15:219–221CrossRefGoogle Scholar
  63. Dickman MB, Podila GK, Kolattukudy PE (1989) Insertion of cutinase gene into a wound pathogen enables it to infect intact host. Nature 342:446–448CrossRefGoogle Scholar
  64. Dumas B, Centis S, Sarrazin N, Esquerré-Tugayé M-T (1999) Use of green fluorescent protein to detect expression of an endopolygalacturonase gene of Colletotrichum lindemuthianum during bean infection. Appl Environ Microbiol 65:1769–1771PubMedGoogle Scholar
  65. Emmett RW, Parbery DG (1975) Appressoria. Annu Rev Phytopathol 13:147–163CrossRefGoogle Scholar
  66. Epstein L, Laccetti L, Staples RC, Hoch HC, Hoose WA (1985) Extracellular proteins associated with induction of differentiation in bean rust urediospore germlings. Phytopathology 75:1073–1076CrossRefGoogle Scholar
  67. Epstein L, Nicholson RL (1997) Adhesion of spores and hyphae to plant surfaces. In: Carroll G, Tudzynski P (eds) The Mycota, vol V, part A. Plant relationships. Springer, Berlin Heidelberg New York, pp 11–25Google Scholar
  68. Flaishman MA, Hwang C-S, Kolattukudy PE (1995) Involvement of protein phosphorylation in the induction of appressorium formation in Colletotrichum gloeosporioides by its host surface wax and ethylene. Physiol Mol Plant Pathol 47:103–117CrossRefGoogle Scholar
  69. Francis SA, Dewey FM, Gurr SJ (1996) The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Pathol 49:201–211CrossRefGoogle Scholar
  70. Frittrang AK, Deising H, Mendgen K (1992) Characterization and partial purification of pectinesterase, a differentiation-specific enzyme of Uromyces viciae-fabae. J Gen Microbiol 138:2213–2218Google Scholar
  71. Gao S, Choi GH, Shain L, Nuss DL (1996) Cloning and targeted disruption of enpg-1, encoding the major in vitro extracellular endopolygalacturonase of the chestnut blight fungus, Cryphonectria parasitica. Appl Environ Microbiol 62:1984–1990PubMedGoogle Scholar
  72. Garrill A, Lew RR, Heath IB (1992) Stretch-activated Ca2+ and Ca2+-activated K+ channels in the hyphal tip plasma membrane of the oomycete Saprolegnia ferax. J Cell Sci 101:721–730Google Scholar
  73. Gay JL, Woods AM (1987) Induced modifications in the plasma membranes of infected cells. In: Pegg GF, Ayers PG (eds) Fungal infection of plants. Cambridge Univ Press, Cambridge, pp 79–91Google Scholar
  74. Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48:335–346CrossRefGoogle Scholar
  75. Girbardt M (1969) Die Ultrastruktur der Apikairegion von Pilzhyphen. Protoplasma 67:413–441CrossRefGoogle Scholar
  76. Gold RE, Mendgen K (1991) Rust basidiospore ger-mlings and disease initiation. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 67–99Google Scholar
  77. Gottleib D (1976) Carbohydrate metabolism and spore germination. In: Weber DJ, Hess WM (eds) The fungal spore. Wiley, New York, pp 141–163Google Scholar
  78. Gow NAR (1995) Tip growth and polarity. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 277–299CrossRefGoogle Scholar
  79. Green JR, Pain NA, Cannell ME, Jones GL, Leckie CP, McCready S, Mendgen K, Mitchell AJ, Callow JA, O’Connell RJ (1995) Analysis of differentiation and development of the specialized infection structures formed by biotrophic fungal plant pathogens using monoclonal antibodies. Can J Bot 73 [Suppl 1]:S408–S417CrossRefGoogle Scholar
  80. Grinberg A, Heath IB (1997) Direct evidence for Ca2+ regulation of hyphal branch induction. Fungal Genet Biol 22:127–139PubMedCrossRefGoogle Scholar
  81. Grove SN, Bracker CE (1970) Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J Bacteriol 104:989–1009PubMedGoogle Scholar
  82. Grove SN, Bracker CE (1978) Protoplasmic changes during zoospore encystment and cyst germination in Pythium aphanidermatum. Exp Mycol 2:51–98CrossRefGoogle Scholar
  83. Grove SN, Sweigard JA (1980) Cytochalasin A inhibits spore germination and hyphal tip growth in Gilbertella persicaria. Exp Mycol 4:239–250CrossRefGoogle Scholar
  84. Grove SN, Bracker CE, Morré DJ (1970) An ultrastructural basis for hyphal tip growth in Pythium ultimum. Am J Bot 57:245–266CrossRefGoogle Scholar
  85. Guan J-L, Chen H-C (1996) Signal transduction in cell-matrix interactions. Int Rev Cytol 168:81–121PubMedCrossRefGoogle Scholar
  86. Gubler F, Hardham AR (1988) Secretion of adhesive material during encystment of Phytophthora cinnamomi zoospores, characterized by immunogold labelling with monoclonal antibodies to components of peripheral vesicles. J Cell Sci 90:225–235Google Scholar
  87. Gubler F, Hardham AR (1990) Protein storage in large peripheral vesicles in Phytophthora zoospores and its breakdown after cyst germination. Exp Mycol 14: 393–404CrossRefGoogle Scholar
  88. Gubler F, Hardham AR (1991) The fate of peripheral vesicles in zoospores of Phytophthora cinnamomi during infection of plants. In: Mendgen K, Lesemann D-E (eds) Electron microscopy of plant pathogens. Springer, Berlin Heidelberg New York, pp 197–210CrossRefGoogle Scholar
  89. Gubler F, Hardham AR, Duniec J (1989) Characterising adhesiveness of Phytophthora cinnamomi zoospores during encystment. Protoplasma 149:24–30CrossRefGoogle Scholar
  90. Hahn M, Neef U, Struck C, Göttfert M, Mendgen K (1997) A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 10:438–445PubMedCrossRefGoogle Scholar
  91. Hamer JE, Howard RJ, Chumley FG, Valent B (1988) A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239:288–290PubMedCrossRefGoogle Scholar
  92. Hardham AR (1992) Cell biology of pathogenesis. Annu Rev Plant Physiol Plant Mol Biol 43:491–526CrossRefGoogle Scholar
  93. Hardham AR (1995) Polarity of vesicle distribution in oomycete zoospores: development of polarity and importance for infection. Can J Bot 73 [Suppl 1]: S400–S407CrossRefGoogle Scholar
  94. Hardham AR, Gubler F (1990) Polarity of attachment of zoospores of a root pathogen and pre-alignment of the emerging germ tube. Cell Biol Int Rep 14:947–956CrossRefGoogle Scholar
  95. Hardham AR, Mitchell HJ (1998) Use of molecular cytology to study the structure and biology of phyto-pathogenic and mycorrhizal fungi. Fungal Genet Biol 24:252–284PubMedCrossRefGoogle Scholar
  96. Hardham AR, Gubler F, Duniec J, Elliott J (1991) A review of methods for the production and use of monoclonal antibodies to study zoosporic plant pathogens. J Microsc 162:305–318CrossRefGoogle Scholar
  97. Hardham AR, Cahill DM, Cope M, Gabor BK, Gubler F, Hyde GJ (1994) Cell surface antigens of Phytophthora spores: biological and taxonomic characterization. Protoplasma 181:213–232CrossRefGoogle Scholar
  98. Heath IB (1994) The cytoskeleton in hyphal growth, organelle movements, and mitosis. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 43–65Google Scholar
  99. Heath IB (1995a) The cytoskeleton. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 99–134CrossRefGoogle Scholar
  100. Heath IB (1995b) Integration and regulation of hyphal tip growth. Can J Bot 73 [Suppl 1]:S131–S139CrossRefGoogle Scholar
  101. Heath IB, Kaminskyj SGW (1989) The organization of tip-growth-related organelles and microtubules revealed by quantitative analysis of freeze-substituted oomycete hyphae. J Cell Sci 93:41–52Google Scholar
  102. Heath IB, Steinberg G (1999) Mechanisms of hyphal tip growth: tube dwelling amoebae revisited. Fungal Genet Biol 28:79–93PubMedCrossRefGoogle Scholar
  103. Heath MC (1976) Ultrastructural and functional similarity of the haustorial neckband of rust fungi and the cas-parian strip of vascular plants. Can J Bot 54:2484–2489CrossRefGoogle Scholar
  104. Hegde Y, Kolattukudy PE (1997) Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea. Physiol Mol Plant Pathol 51:75–84CrossRefGoogle Scholar
  105. Heiler S, Mendgen K, Deising H (1993) Cellolytic enzymes of the obligately biotrophic rust fungus Uromyces viciae-fabae are regulated differentiation-specifically. Mycol Res 97:77–85CrossRefGoogle Scholar
  106. Hemmes DE, Hohl HR (1971) Ultrastructural aspects of encystation and cyst-germination in Phytophthora parasitica. J Cell Sci 9:175–191PubMedGoogle Scholar
  107. Hill TW, Mullins JT (1980) Hyphal tip growth in Achlya. I. Cytoplasmic organization. Can J Microbiol 26:1132–1140PubMedCrossRefGoogle Scholar
  108. Hippe-Sanwald S, Marticke KH, Kieliszewski MJ, Somerville SC (1994) Immunogold localization of THRGP-like epitopes in the haustorial interface of obligate, biotrophic fungi on monocots. Protoplasma 178:138–155CrossRefGoogle Scholar
  109. Hoch HC, Staples RC (1987) Structural and chemical changes among the rust fungi during appressorium development. Annu Rev Phytopathol 25:231–247CrossRefGoogle Scholar
  110. Hoch HC, Staples RC (1991) Signaling for infection structure formation in fungi. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 25–46Google Scholar
  111. Hoch HC, Bourett TM, Staples RC (1986) Inhibition of cell differentiation in Uromyces with D20 and taxol. Eur J Cell Biol 41:290–297Google Scholar
  112. Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED (1987a) Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235:1659–1662PubMedCrossRefGoogle Scholar
  113. Hoch HC, Tucker BE, Staples RC (1987b) An intact microtubule cytoskeleton is necessary for mediation of the signal for cell differentiation in Uromyces. Eur J Cell Biol 45:209–218Google Scholar
  114. Hoch HC, Bojko RJ, Comeau GL, Lilienfeld DA (1995) Microfabricated surfaces in signaling for cell growth and differentiation in fungi. In: Hoch HC, Jelinski LW, Craighead H (eds) Nanofabrication and biosystems: integrating materials science, engineering, and biology. Cambridge Univ Press, Cambridge, pp 315–334Google Scholar
  115. Horak J (1986) Amino acid transport in eucaryotic microorganisms. Biochem Biophys Acta 864:223–256PubMedCrossRefGoogle Scholar
  116. Howard RJ (1994) Cell biology of pathogenesis. In: Zeigler RS, Leong SA, Teng PS (eds) Rice blast disease. CAB International, Wallingford, pp 3–22Google Scholar
  117. Howard RJ (1997) Breaching the outer barriers — cuticle and cell wall penetration. In: Carroll G, Tudzynski P (eds) The Mycota, vol V, part A. Plant relationships. Springer, Berlin Heidelberg New York, pp 43–60Google Scholar
  118. Howard RJ, Ferrari MA (1989) Role of melanin in appressorium function. Exp Mycol 13:403–418CrossRefGoogle Scholar
  119. Howard RJ, Valent B (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grísea. Annu Rev Microbiol 50:491–512PubMedCrossRefGoogle Scholar
  120. Howard RJ, Bourett TM, Ferrari MA (1991a) Infection by Magnaporthe: an in vitro analysis. In: Mendgen K, Lesemann D-E (eds) Electron microscopy of plant pathogens. Springer, Berlin Heidelberg New York, pp 251–264CrossRefGoogle Scholar
  121. Howard RJ, Ferrari MA, Roach DH, Money NP (1991b) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA 88:11281–11284PubMedCrossRefGoogle Scholar
  122. Hughes HB, Carzaniga R, Rawlings SL, Green JR, O’Connell RJ (1999) Spore surface glycoproteins of Colletotrichum lindemuthianum are recognized by a monoclonal antibody which inhibits adhesion to polystyrene. Microbiology 145:1927–1936PubMedCrossRefGoogle Scholar
  123. Hyde GJ, Hardham AR (1993) Microtubules regulate the generation of polarity in zoospores of Phytophthora cinnamomi. Eur J Cell Biol 62:75–85PubMedGoogle Scholar
  124. Hyde GJ, Heath IB (1995) Ca2+-dependent polarization of axis establishment in the tip-growing organism, Saprolegnia ferax, by gradients of the ionophore A23187. Eur J Cell Biol 67:356–362PubMedGoogle Scholar
  125. Hyde GJ, Davies D, Perasso L, Cole L, Ashford AE (1999) Microtubules, but not actin microfilaments, regulate vacuole motility and morphology in hyphae of Pisolithus tinctorius. Cell Motil Cytoskeleton 42:114–124PubMedCrossRefGoogle Scholar
  126. Inoue S, Turgeon BG, Yoder OC, Aist JR (1998) Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration. J Cell Sci 111:1555–1566PubMedGoogle Scholar
  127. Jackson SL, Heath IB (1990) Evidence that actin reinforces the extensible hyphal apex of the oomycete Saprolegnia ferax. Protoplasma 157:144–53CrossRefGoogle Scholar
  128. Jelitto TC, Page HA, Read ND (1994) Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus, Magnaporthe grisea. Planta 194:471–477CrossRefGoogle Scholar
  129. Jones MJ, Epstein L (1989) Adhesion of Nectria haematococca macroconidia. Physiol Mol Plant Pathol 35: 453–461CrossRefGoogle Scholar
  130. Kaminskyj SGW, Heath IB (1996) Studies on Saprolegnia ferax suggest the general importance of the cytoplasm in determining hyphal morphology. Mycologia 88: 20–37CrossRefGoogle Scholar
  131. Kawamura C, Moriwaki J, Kimura N, Fujita Y, Fuji S, Hirano T Koizumi S, Tsuge T (1997) The melanin biosynthesis genes of Alternaria alternata can restore pathogenicity of the melanin-deficient mutants of Magnaporthe grisea. Mol Plant Microbe Interact 10: 446–453PubMedCrossRefGoogle Scholar
  132. Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. Fungal Genet Biol 23:18–33PubMedCrossRefGoogle Scholar
  133. Kunoh H, Nicholson RL, Kobayashi I (1991) Extracellular materials of fungal structures: their significance at prepenetration stages of infection. In: Mendgen K, Lesemann D-E (eds) Electron microscopy of plant pathogens. Springer, Berlin Heidelberg New York, pp 223–234CrossRefGoogle Scholar
  134. Kuo K, Hoch HC (1996) Germination of Phyllosticta ampelicida pycnidiospores: prerequisite of adhesion to the substratum and the relationship of substratum wettability. Fungal Genet Biol 20:18–29PubMedCrossRefGoogle Scholar
  135. Kwon YH, Epstein L (1993) A 90-kDa glycoprotein associated with adhesion of Nectria haematococca macroconidia to substrata. Mol Plant Microbe Interact 6: 481–487CrossRefGoogle Scholar
  136. Kwon YH, Epstein L (1997a) Involvement of the 90-kDa glycoprotein in adhesion of Nectria haematococca macroconidia. Physiol Mol Plant Pathol 51:287–303CrossRefGoogle Scholar
  137. Kwon YH, Epstein L (1997b) Isolation and composition of the 90kDa glycoprotein associated with adhesion of Nectria haematococca macroconidia. Physiol Mol Plant Pathol 51:63–74CrossRefGoogle Scholar
  138. Kwon YH, Hoch HC (1991) Temporal and spatial dynamics of appressorium formation in Uromyces appendiculartus. Exp Mycol 15:116–131CrossRefGoogle Scholar
  139. Kwon YH, Hoch HC, Staples RC (1991a) Cytoskeletal organization in Uromyces urediospore germling apices during appressorium formation. Protoplasma 165:37–50CrossRefGoogle Scholar
  140. Kwon YH, Hoch HC, Aist JR (1991b) Initiation of appressorium formation in Uromyces appendiculatus: organization of the apex, and the responses involving microtubules and apical vesicles. Can J Bot 69:2560–2573CrossRefGoogle Scholar
  141. Langford GM (1995) Actin- and microtubule-dependent organelle motors: interrelationships between the two motility systems. Curr Opin Cell Biol 7:82–88PubMedCrossRefGoogle Scholar
  142. Lee Y-H, Dean RA (1993) cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell 5:693–700PubMedGoogle Scholar
  143. Lee Y-H, Dean RA (1994) Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grísea. FEMS Microbiol Lett 115:71–76CrossRefGoogle Scholar
  144. Lehmler C, Steinberg G, Snetselaar KM, Schliwa M, Kahmann R, Bölker M (1997) Identification of a motor protein required for filamentous growth in Ustílago mayáis. EMBO J 16:3464–3473PubMedCrossRefGoogle Scholar
  145. Levina NN, Lew RR, Heath IB (1994) Cytoskeletal regulation of ion channel distribution in the tip-growth organism Saprolegnia ferax. J Cell Sci 107:127–134PubMedGoogle Scholar
  146. Littlefield LJ, Bracker CE (1972) Ultrastructural specialization at the host-pathogen interface in rust-infected flax. Protoplasma 74:271–305CrossRefGoogle Scholar
  147. Liu S, Dean RA (1997) G protein α subunit genes control growth, development, and pathogenicity of Magnaporthe grísea. Mol Plant Microbe Interact 10:1075–1086PubMedCrossRefGoogle Scholar
  148. Liu ZL, Szabo LJ, Bushnell WR (1993) Molecular cloning and analysis of abundant and stage-specific mRNAs from Puccinia graminis. Mol Plant Microbe Interact 6:84–91PubMedCrossRefGoogle Scholar
  149. Liu ZM, Kolattukudy PE (1999) Early expression of the calmodulin gene, which precedes appressorium formation in Magnaporthe grisea, is inhibited by self-inhibitors and requires surface attachment. J Bacteriol 181:3571–3577PubMedGoogle Scholar
  150. López-Franco R, Bracker CE (1996) Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195:90–111CrossRefGoogle Scholar
  151. Lovett JS (1975) Growth and differentiation of the water mold Blastocladiella emersomi: cytodifferentiation and the role of ribonucleic acid and protein synthesis. Bacteriol Rev 39:345–404PubMedGoogle Scholar
  152. Lovett JS (1976) Regulation of protein metabolism during spore germination. In: Weber DJ, Hess WM (eds) The fungal spore. Wiley, New York, pp 190–240Google Scholar
  153. Lucas J, Knights I (1987) Spores on leaves: endogenous and exogenous control of development. In: Pegg GF, Ayres PG (eds) Fungal infection of plants. Cambridge Univ Press, Cambridge, pp 45–59Google Scholar
  154. Mackie AJ, Roberts AM, Callow JA, Green JR (1991) Molecular differentiation in pea powdery-mildew haustoria. Planta 183:399–408CrossRefGoogle Scholar
  155. Mackie AJ, Roberts AM, Green JR, Callow JA (1993) Glycoproteins recognised by monoclonal antibodies UB7, UB8 and UB10 are expressed early in the development of pea powdery mildew haustoria. Physiol Mol Plant Pathol 43:135–146CrossRefGoogle Scholar
  156. Macko V (1981) Inhibitors and stimulants of spore germination and infection structure formation in fungi. In: Turian G, Hohl HR (eds) The fungal spore: morphogenetic controls. Academic Press, London, pp 565–584Google Scholar
  157. MacLeod H, Horgen PA (1979) Germination of the asexual spores of the aquatic fungus, Achlya bisexualis. Exp Mycol 3:70–82CrossRefGoogle Scholar
  158. Maiti IB, Kolattukudy PE (1979) Prevention of fungal infection of plants by specific inhibition of cutinase. Science 205:507–508PubMedCrossRefGoogle Scholar
  159. Manners JM, Gay JL (1978) Uptake of 14C photosynthates from Pisum sativum by haustoria of Erysiphe pisi. Physiol Plant Pathol 12:199–209CrossRefGoogle Scholar
  160. Manners JM, Gay JL (1980) Autoradiography of haustoria of Erysiphe pisi. J Gen Microbiol 116:529–533Google Scholar
  161. Manners JM, Gay JL (1982) Transport, translocation and metabolism of 14C-photosynthates at the host-parasite interface of Pisum sativum and Erysiphe pisi. New Phytol 91:221–244CrossRefGoogle Scholar
  162. Manners JM, Gay JL (1983) The host-parasite interface and nutrient transfer in biotrophic parasitism. In: Callow JA (ed) Biochemical plant pathology. Wiley-Interscience, Chichester, pp 163–195Google Scholar
  163. Martin JT, Jumper BE (1970) The cuticles of plants. Arnold, EdinburghGoogle Scholar
  164. McGoldrick CA, Gruver C, May GS (1995) myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J Cell Biol 128:577–587PubMedCrossRefGoogle Scholar
  165. Mendgen K (1981) Nutrient uptake in rust fungi. Phytopathology 71:983–989CrossRefGoogle Scholar
  166. Mendgen K, Deising H (1993) Infection structures of fungal plant pathogens — a cytological and physiological evaluation. New Phytol 124:193–213CrossRefGoogle Scholar
  167. Mendgen K, Bachern U, Stark-Urnau M, Xu H (1995) Secretion and endocytosis at the interface of plants and fungi. Can J Bot 73 [Suppl 1]:S640-S648CrossRefGoogle Scholar
  168. Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386PubMedCrossRefGoogle Scholar
  169. Mercure EW, Leite B, Nicholson RL (1994a) Adhesion of ungerminated conidia of Colletotrichum graminicola to artificial hydrophobic surfaces. Physiol Mol Plant Pathol 45:421–440CrossRefGoogle Scholar
  170. Mercure EW, Kunoh H, Nicholson RL (1994b) Adhesion of Colletotrichum graminicola conidia to corn leaves: a requirement for disease development. Physiol Mol Plant Pathol 45:407–420CrossRefGoogle Scholar
  171. Mims CW, Richardson EA (1989) Ultrastructure of appressorium development by basidiospore germlings of the rust fungus Gymnosporangium juniperi-virginianae. Protoplasma 148:111–119CrossRefGoogle Scholar
  172. Mims CW, Taylor J, Richardson EA (1989) Ultrastructure of the early stages of infection of peanut leaves by the rust fungus Puccinia arachidis. Can J Bot 67:3570–3579CrossRefGoogle Scholar
  173. Mitchell AJ, Hutchinson KA, Pain NA, Callow JA, Green JR (1997) A monoclonal antibody that recognizes a carbohydrate epitope on N-linked glycoproteins restricted to a subset of chitin-rich fungi. Mycol Res 101:73–79CrossRefGoogle Scholar
  174. Mitchell RT, Deacon JW (1986) Chemotropism of germ-tubes from zoospore cysts of Pythium spp. Trans Br Mycol Soc 86:233–237CrossRefGoogle Scholar
  175. Moloshok TD, Leinhos GME, Staples RC, Hoch HC (1993) The autogenic extracellular environment of Uromyces appendiculatus urediospore germlings. Mycologia 85: 392–400CrossRefGoogle Scholar
  176. Money NP (1994) Osmotic adjustment and the role of turgor in mycelial fungi. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 67–88Google Scholar
  177. Money NP, Howard RJ (1996) Confirmation of a link between fungal pigmentation, turgor pressure, and pathogenicity using a new method of turgor measurement. Exp Mycol 20:217–227Google Scholar
  178. Murdoch LJ, Hardham AR (1998) Components in the haustorial wail of the flax rust fungus, Melampsora lini, are labelled by three anti-calmodulin monoclonal antibodies. Protoplasma 201:180–193CrossRefGoogle Scholar
  179. Murdoch LJ, Kobayashi I, Hardham AR (1998) Production and characterisation of monoclonal antibodies to cell wall components of the flax rust fungus. Eur J Plant Pathol 104:331–346CrossRefGoogle Scholar
  180. Murphy JM, Walton JD (1996) Three extracellular proteases from Cochliobolus carbonum: cloning and targeted disruption of ALP1. Mol Plant Microbe Interact 9:290–297PubMedCrossRefGoogle Scholar
  181. Nicholson RL (1996) Adhesion of fungal propagules. In: Nicole M, Gianinazzi-Pearson V (eds) Histology, ultrastructure and molecular cytology of plant-microorganism interactions. Kluwer, Dordrecht, pp 117–134CrossRefGoogle Scholar
  182. Nicholson RL, Epstein L (1991) Adhesion of fungi to the plant surface. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 3–23Google Scholar
  183. Nicholson RL, Kunoh H, Shiraishi T, Yamada T (1993) Initiation of the infection process by Erysiphe graminis: conversion of the conidial surface from hydrophobicity to hydrophilicity and influence of the conidial exudate on the hydrophobicity of the barley leaf surface. Physiol Mol Plant Pathol 43:307–318CrossRefGoogle Scholar
  184. Nolan RA, Bal AK (1974) Cellulase localization in hyphae of Achlya ambisexualis. J Bacteriol 117:840–843PubMedGoogle Scholar
  185. O’Connell RJ (1987) Absence of a specialized interface between intracellular hyphae of Colletotrichum linde-muthianum and cells of Phaseolus vulgaris. New Phytol 107:725–734CrossRefGoogle Scholar
  186. O’Connell RJ, Bailey JA (1991) Hemibiotrophy in Colletotrichum lindemuthianum. In: Mendgen K, Lesemann DE (eds) Electron microscopy of plant pathogens. Springer, Berlin Heidelberg New York, pp 211–22CrossRefGoogle Scholar
  187. O’Connell RJ, Ride JP (1990) Chemical detection and ultrastructural localization of chitin in cell walls of Colletotrichum lindemuthianum. Physiol Mol Plant Pathol 37:39–53CrossRefGoogle Scholar
  188. O’Connell RJ, Pain NA, Bailey JA, Mendgen K, Green JR (1996a) Use of monoclonal antibodies to study differentiation of Colletotrichum infection structures. In: Nicole M, Gianinazzi-Pearson V (eds) Histology, ultrastructure and molecular cytology of plant-microorganism interactions. Kluwer, Dordrecht, pp 79–97CrossRefGoogle Scholar
  189. O’Connell RJ, Pain NA, Hutchison KA, Jones GL, Green JR (1996b) Ultrastructure and composition of the cell surfaces of infection structures formed by the fungal plant pathogen Colletotrichum lindemuthianum. J Microsc 181:204–212CrossRefGoogle Scholar
  190. Pain NA, O’Connell RJ, Bailey JA, Green JR (1992) Monoclonal antibodies which show restricted binding to four Colletotrichum species: C. lindemuthianum, C. malvarum, C. orbiculare and C. trifolii. Physiol Mol Plant Pathol 40:111–126CrossRefGoogle Scholar
  191. Pain NA, O’Connell RJ, Mendgen K, Green JR (1994) Identification of glycoproteins specific to biotrophic intracellular hyphae formed in the Colletotrichum lindemuthianum-bean interaction. New Phytol 127: 233–242CrossRefGoogle Scholar
  192. Pain NA, O’Connell RJ, Green JR (1995) A plasma membrane-associated protein is a marker for differentiation and polarisation of Colletotrichum lindemuthianum appressoria. Protoplasma 188:1–11CrossRefGoogle Scholar
  193. Pain NA, Green JR, Jones GL, O’Connell RJ (1996) Composition and organisation of extracellular matrices around germ tubes and appressoria of Colletotrichum lindemuthianum. Protoplasma 190:119–130CrossRefGoogle Scholar
  194. Paktitis S, Grant B, Lawrie A (1986) Surface changes in Phytophthora palmivora zoospores following induced differentiation. Protoplasma 135:119–129CrossRefGoogle Scholar
  195. Pascholati SF, Yoshioka H, Kunoh H, Nicholson RL (1992) Preparation of the infection court by Erysiphe graminis f. sp. hordei: cutinase is a component of the conidial exudate. Physiol Mol Plant Pathol 41:53–59CrossRefGoogle Scholar
  196. Penington CJ, Iser JR, Grant BR, Gayler KR (1989) Role of RNA and protein synthesis in stimulated germination of zoospores of the pathogenic fungus Phytophthora palmivora. Exp Mycol 13:158–168CrossRefGoogle Scholar
  197. Perfect SE, O’Connell RJ, Green EF, Doering-Saad C, Green JR (1998) Expression cloning of a fungal proline-rich glycoprotein specific to the biotrophic interface formed in the Colletotrichum-bean interaction. Plant J 15:273–279PubMedCrossRefGoogle Scholar
  198. Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum — a model genus for studies on pathology and fungal-plant interactions. Fungal Genet Biol 27:186–198PubMedCrossRefGoogle Scholar
  199. Perpetua NS, Kubo Y, Yasuda N, Takano Y, Furusawa I (1996) Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium. Mol Plant Microbe Interact 9:323–329PubMedCrossRefGoogle Scholar
  200. Pickett-Heaps JD, Klein AG (1998) Tip growth in plant cells may be amoeboid and not generated by turgor pressure. Proc R Soc Lond B Biol Sci 265:1453–1459CrossRefGoogle Scholar
  201. Podila GK, Rosen E, San Francisco MJD, Kolattukudy PE (1995) Targeted secretion of cutinase in Fusarium solani f. sp. pisi and Colletotrichum gloeosporioides. Phytopathology 85:238–242CrossRefGoogle Scholar
  202. Powell MJ, Bracker CE (1977) Isolation of zoospore organelles from Phytophthora palmivora. Proc 2nd Int Mycol Congr, Tampa, FL, p 533Google Scholar
  203. Pryce-Jones E, Carver T, Gurr SJ (1999) The roles of cellulase enzymes and mechanical force in host penetration by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Pathol 55:175–182CrossRefGoogle Scholar
  204. Read ND (1991) Low-temperature scanning electron microscopy of fungi and fungus-plant interactions. In: Mendgen K, Lesemann D-E (eds) Electron microscopy of plant pathogens. Springer, Berlin Heidelberg New York, pp 17–29CrossRefGoogle Scholar
  205. Read ND, Kellock LJ, Knight H, Trewavas AJ (1992) Contact sensing during infection by fungal pathogens. In: Callow JA, Green JR (eds) Perspectives in plant cell recognition. Cambridge Univ Press, Cambridge, pp 137–172CrossRefGoogle Scholar
  206. Read ND, Kellock LJ, Collins TJ, Gundlach AM (1997) Role of topography sensing for infection-structure differentiation in cereal rust fungi. Planta 202:163–170CrossRefGoogle Scholar
  207. Reisener HJ (1976) Lipid metabolism of fungal spores during sporogenesis and germination. In: Weber DJ, Hess WM (eds) The fungal spore. Wiley, New York, pp 166–185Google Scholar
  208. Riquelme M, Reynaga-Peña CG, Gierz G, Bartnicki-García S (1998) What determines growth direction in fungal hyphae? Fungal Genet Biol 24:101–109PubMedCrossRefGoogle Scholar
  209. Roberson RW, Fuller MS (1988) Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma 146:143–149CrossRefGoogle Scholar
  210. Roberson RW, Fuller MS (1990) Effects of the demethy-lase inhibitor, cyproconazole, on hyphal tip cells of Sclerotium rolfsii. II. An electron microscope study. Exp Mycol 14:124–135CrossRefGoogle Scholar
  211. Roberson RW, Vargas MM (1994) The tubulin cytoskeleton and its sites of nucleation in hyphal tips of Allomyces macrogynus. Protoplasma 182:19–31CrossRefGoogle Scholar
  212. Roberts AM, Mackie AJ, Hathaway V, Callow JA, Green JR (1993) Molecular differentiation in the extrahaus-torial membrane of pea powdery mildew haustoria at early and late stages of development. Physiol Mol Plant Pathol 43:147–160CrossRefGoogle Scholar
  213. Robinson PM (1973) Oxygen — positive chemotropic factor for fungi? New Phytol 72:1349–1356CrossRefGoogle Scholar
  214. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Biol 12:697–715CrossRefGoogle Scholar
  215. Russo GM, Dahlberg KR, Van Etten JL (1982) Identification of a development-specific protein in sclerotia of Sclerotinia sclerotiorum. Exp Mycol 6:259–267CrossRefGoogle Scholar
  216. Sachs MS, Yanofsky C (1991) Developmental expression of genes involved in conidiation and amino acid biosynthesis in Neurospora crassa. Dev Biol 148:117–128PubMedCrossRefGoogle Scholar
  217. Satiat-Jeunemaitre B, Cole L, Bourett T, Howard R, Hawes C (1996) Brefeldin A effects in plant and fungal cells: something new about vesicle trafficking? J Microsc 181:162–177PubMedCrossRefGoogle Scholar
  218. Schaeffer HJ, Leykam J, Walton JD (1994) Cloning and targeted gene disruption of EXG1, encoding exo-β1;,3-glucanase, in the phytopathogenic fungus Cochliobo-lus carbonum. Appl Environ Microbiol 60:594–598PubMedGoogle Scholar
  219. Scherer GFE, vom Dorp B, Schöllman C, Volkmann D (1992) Proton-transport activity, sidedness, and morphometry of tonoplast and plasma-membrane vesicles purified by free-flow electrophoresis from roots of Lepidium sativum L. and hypocotyls of Cucurbita pepo L. Planta 186:483–494CrossRefGoogle Scholar
  220. Scott-Craig JS, Panaccione DG, Cervone F, Walton JD (1990) Endopolygalacturonase is not required for pathogenicity of Cochliobolus carbonum on maize. Plant Cell 2:1191–1200PubMedGoogle Scholar
  221. Scott-Craig JS, Cheng Y-Q, Cervone F, De Lorenzo G, Pitkin JW, Walton JD (1998) Targeted mutants of Cochliobolus carbonum lacking the two major extracellular polygalacturonases. Appl Environ Microbiol 64:1497–1503PubMedGoogle Scholar
  222. Shaw BD, Hoch HC (1999) The pycnidiospore of Phyllosticta ampelicida: surface properties involved in substratum attachment and germination. Mycol Res 103: 915–924CrossRefGoogle Scholar
  223. Shaw BD, Kuo K-C, Hoch HC (1998) Germination and appressorium development of Phyllosticta ampelicida pycnidiospores. Mycologia 90:258–268CrossRefGoogle Scholar
  224. Shaykh M, Soliday C, Kolattukudy PE (1977) Proof for the production of cutinase by Fusarium solani f. pisi during penetration into its host, Pisum sativum. Plant Physiol 60:170–172PubMedCrossRefGoogle Scholar
  225. Shepherd VA, Orlovich DA, Ashford AE (1993) A dynamic continuum of pleomorphic tubules and vacuoles in growing hyphae of a fungus. J Cell Sci 104:495–507Google Scholar
  226. Shieh M-T, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA (1997) Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl Environ Microbiol 63: 3548–3552PubMedGoogle Scholar
  227. Sietsma JH, Wessels JGH (1994) Apical wall biogenesis. In: Wessels JGH Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 125–141Google Scholar
  228. Söderhall K, Cerenius L (1983) Protein and nucleic acid synthesis during germination of the asexual spores of the aquatic fungus, Aphanomyces astaci. Physiol Plant 58:13–17CrossRefGoogle Scholar
  229. Spencer-Phillips PTN, Gay JL (1981) Domains of ATPase in plasma membranes and transport through infected plant cells. New Phytol 89:393–400CrossRefGoogle Scholar
  230. Sposato P, Ahn J-H, Walton JD (1995) Characterization and disruption of a gene in the maize pathogen Cochliobolus carbonum encoding a cellulase lacking a cellulose binding domain and hinge region. Mol Plant Microbe Interact 8:602–609PubMedCrossRefGoogle Scholar
  231. Sreedhar L, Kobayashi DY, Bunting TE, Hillman BI, Belanger FC (1999) Fungal proteinase expression in the interaction of the plant pathogen Magnaporthe poae with its host. Gene 235:121–129PubMedCrossRefGoogle Scholar
  232. Srinivasan S, Vargas MM, Roberson RW (1996) Functional, organizational, and biochemical analysis of actin in hyphal tip cells of Allomyces macrogynus. Mycologia 88:57–70CrossRefGoogle Scholar
  233. Stahl DJ, Schäfer W (1992) Cutinase is not required for fungal pathogenicity on pea. Plant Cell 4:621–629PubMedGoogle Scholar
  234. Staples RC, Hoch HC (1997) Physical and chemical cues for spore germination and appressorium formation by fungal pathogens. In: Carroll G, Tudzynski P (eds) The Mycota, vol V, part A. Plant relationships. Springer, Berlin Heidelberg New York, pp 27–40Google Scholar
  235. Stark-Urnau M, Mendgen K (1995) Sequential deposition of plant glycoproteins and polysaccharides at the host-parasite interface of Uromyces vignae and Vigna sinensis. Evidence for endocytosis and secretion. Protoplasma 186:1–11CrossRefGoogle Scholar
  236. Strader CD, Fong TM, Tota MR, Underwood D, Dixon RAF (1994) Structure and function of G protein-coupled receptors. Annu Rev Biochem 63:101–132PubMedCrossRefGoogle Scholar
  237. Struck C, Hahn M, Mendgen K (1996) Plasma membrane H+-ATPase activity in spores, germ tubes, and haustoria of the rust fungus Uromyces viciae-fabae. Fungal Genet Biol 20:30–35PubMedCrossRefGoogle Scholar
  238. Struck C, Siebels C, Rommel O, Wernitz M, Hahn M (1998) The plasma membrane H+-ATPase from the biotrophic rust fungus Uromyces fabae: molecular characterization of the gene (PMA1) and functional expression of the enzyme in yeast. Mol Plant Microbe Interact 11:458–465PubMedCrossRefGoogle Scholar
  239. Sugui JA, Leite B, Nicholson RL (1998) Partial characterization of the extracellular matrix released onto hydrophobic surfaces by conidia and conidial germlings of Colletotrichum graminicola. Physiol Mol Plant Pathol 52:411–425CrossRefGoogle Scholar
  240. Sweigard JA, Chumley FG, Valent B (1992) Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232:183–190PubMedGoogle Scholar
  241. 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
  242. Talbot NJ, Kershaw MJ, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8:985–999PubMedGoogle Scholar
  243. Taylor J, Mims CW (1991) Fungal development and host cell responses to the rust fungus Puccinia substriata var. índica in seedling and mature leaves of susceptible and resistant pearl millet. Can J Bot 69:1207–1219CrossRefGoogle Scholar
  244. Ten Have A, Mulder W, Visser J, van Kan JAL (1998) The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11:1009–1016PubMedCrossRefGoogle Scholar
  245. Terhune BT, Hoch HC (1993) Substrate hydrophobicity and adhesion of Uromyces urediospores and germlings. Exp Mycol 17:241–252CrossRefGoogle Scholar
  246. Terhune BT, Bojko RJ, Hoch HC (1993) Deformation of stomatal guard cell lips and microfabricated artificial topographies during appressorium formation by Uromyces. Exp Mycol 17:70–78CrossRefGoogle Scholar
  247. Thevelein JM (1996) Regulation of trehalose metabolism and its relevance to cell growth and function. In: Brambl R, Marzluf GA (eds) The mycota, vol III. Biochemistry and molecular biology. Springer, Berlin Heidelberg New York, pp 395–420Google Scholar
  248. Thines E, Eilbert F, Sterner O, Anke H (1997) Glisoprenin A, an inhibitor of the signal transduction pathway leading to appressorium formation in germinating conidia of Magnaporthe grísea on hydrophobic surfaces. FEMS Microbiol Lett 151:219–224CrossRefGoogle Scholar
  249. Ton-ThatTC, Rossier C, Barja F,Turian G, Roos U-P (1988) Induction of multiple germ tubes in Neurospora crassa by antitubulin agents. Eur J Cell Biol 46:68–79PubMedGoogle Scholar
  250. Van Etten JL, Dunkle LD, Knight RH (1976) Nucleic acids and fungal spore germination. In: Weber DJ, Hess WM (eds) The fungal spore. Wiley, New York, pp 244–299Google Scholar
  251. Van Etten JL, Freer SN, McCune BK (1979) Presence of a major (storage?) protein in dormant spores of the fungus Botryodiplodia theobromae. J Bacteriol 138: 650–652PubMedGoogle Scholar
  252. van Kan JAL, Van’t Klooster JW, Wagemakers CAM, Dees DCT, van der Vlugt-Bergmans CJB (1997) Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol Plant Microbe Interact 10:30–38PubMedCrossRefGoogle Scholar
  253. Viret O, Tott L, Chapela IH, Petrini O (1994) The role of the extracellular sheath in recognition and attachment of conidia of Discula umbrinella (Berk. & Br.) Morelet to the host surface. New Phytol 127:123–131CrossRefGoogle Scholar
  254. Wang M-C, Bartnicki-Garcia S (1980) Distribution of mycolaminarans and cell wall β-glucans in the life cycle of Phytophthora. Exp Mycol 4:269–280CrossRefGoogle Scholar
  255. Warwar V, Dickman MB (1996) Effects of calcium and calmodulin on spore germination and appressorium development in Colletotrichum trifola. Appl Environ Microbiol 62:74–79PubMedGoogle Scholar
  256. Wattad C, Kobiler D, Dinoor A, Prusky D (1997) Pectate lyase of Colletotrichum gloeosporioides attacking avocado fruits: cDNA cloning and involvement in pathogenicity. Physiol Mol Plant Pathol 50:197–212CrossRefGoogle Scholar
  257. Welter K, Müller M, Mendgen K (1988) The hyphae of Uromyces appendiculatus within the leaf tissue after high pressure freezing and freeze substitution. Protoplasma 147:91–99CrossRefGoogle Scholar
  258. Wessels JGH (1996) Fungal hydrophobins: proteins that function at an interface. Trends Plant Sci 1:9–14CrossRefGoogle Scholar
  259. Wessels JGH (1999) Fungi in their own right. Fungal Genet Biol 27:134–145PubMedCrossRefGoogle Scholar
  260. Woloshuk CP, Sisler HD, Vigil EL (1983) Action of the antipenetrant, tricyclazole, on appressoria of Pyricularia oryzae. Physiol Plant Pathol 22:245–259Google Scholar
  261. Woods AM, Gay JL (1983) Evidence for a neckband delimiting structural and physiological regions of the host plasma membrane associated with haustoria of Albugo candida. Physiol Plant Pathol 23:73–88CrossRefGoogle Scholar
  262. Woods AM, Gay JL (1987) The interface between haustoria of Puccinia poarum (monokaryon) and Tussilago farfara. Physiol Mol Plant Pathol 30:167–185CrossRefGoogle Scholar
  263. Wynn WK (1976) Appressorium formation over stomates by the bean rust fungus: response to a surface contact stimulus. Phytopathology 66:136–146CrossRefGoogle Scholar
  264. Wynn WK (1981) Tropic and taxic responses of pathogens to plants. Annu Rev Phytopathol 19:237–255CrossRefGoogle Scholar
  265. Xiao J-Z, Watanabe T, Kamakura T, Ohshima A, Yamaguchi I (1994) Studies on cellular differentiation of Magnaporthe grisea. Physicochemical aspects of substratum surfaces in relation to appressorium formation. Physiol Mol Plant Pathol 44:227–236CrossRefGoogle Scholar
  266. Xu H, Mendgen K (1997) Targeted cell wall degradation at the penetration site of cowpea rust basidiosporelings. Mol Plant Microbe Interact 10:87–94CrossRefGoogle Scholar
  267. Yamaoka N, Takeuchi Y (1999) Morphogenesis of the powdery mildew fungus in water. 4. The significance of conidium adhesion to the substratum for normal appressorium development in water. Physiol Mol Plant Pathol 54:145–154CrossRefGoogle Scholar
  268. Yamashita RA, May GS (1998) Motoring along the hyphae: molecular motors and the fungal cytoskeleton. Curr Opin Cell Biol 10:74–79PubMedCrossRefGoogle Scholar
  269. Yang Z, Dickman MB (1997) Regulation of cAMP and cAMP dependent protein kinase during conidial germination and appressorium formation in Colletotrichum trifola. Physiol Mol Plant Pathol 50: 117–127CrossRefGoogle Scholar
  270. Yao C, Köller W (1995) Diversity of cutinases from plant pathogenic fungi: different cutinases are expressed during saprophytic and pathogenic stages of Alternaría brassicicola. Mol Plant Microbe Interact 8: 122–130CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • Adrienne R. Hardham
    • 1
  1. 1.Plant Cell Biology Group, Research School of Biological SciencesThe Australian National UniversityCanberraAustralia

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