Studies on Saprolegnia ferax suggest the general importance of the cytoplasm in determining hyphal morphology

Mycologia

Volumn 88, Issue 1, 1996, Pages 20-37

  Kaminskyj, Susan G W ^a,b   Heath, I Brent ^a  

^a YORK UNIVERSITY   (Canada)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Actin; Cytoplasmic migration; Cytoskeleton; Integrin; Saprolegnia ferax; Spectrin; Tensegrity; Tip growth

Indexed keywords

EID: 0030026297     PISSN: 00275514     EISSN: None     Source Type: Journal    
DOI: 10.2307/3760781     Document Type: Article

References (140)

1. Adams, A. E. M., and J. R. Pringle. 1984. Relationship of actin and tubulin distribution to bud growth in wildtype and morphogenetic mutant Saccharomyces cerevisiae. J. Cell Biol. 98: 934-945.
2. Adams, R. J., and T. D. Pollard. 1989. Binding of myosin I to membrane lipids. Nature 340: 565-568.
3. Aist, J. R., and C. J. Bayles. 1991. Ultrastructural basis of mitosis in the fungus Nectria hematococca (sexual stage of Fusarium solani). I. Asters. Protoplasma 161: 111-122.
4. _, and M. W. Berns. (1981). Mechanics of chromosome separation during mitosis in Fusarium (Fungi imperfecti): new evidence from ultrastructural and laser microbeam experiments. J. Cell Biol. 91: 446-458.
5. Allen, R. D. 1961. Amoeboid movement. Pp. 135-216.In: The Cell. Volume II. Cells and their component parts. Academic Press, New York and London.
6. Baines, I. C., H. Brzeska, and E. D. Korn. 1992. Differential localization of Acanthamoeba myosin I isoforms. J. Cell Biol. 119: 1193-1203.
7. Bartnicki-Garcia, S. 1990. Role of vesicles in apical growth and a new mathematical model of hyphal morphogenesis. Pp. 211-232. In: Tip Growth in Plant and Fungal Cells. Ed., I. B. Heath. Academic Press, Toronto and New York.
8. Bennett, V. 1990. Spectrin: a structural mediator between diverse plasma membrane proteins and the cytoplasm. Curr. Opin. Cell Biol. 2: 51-56.
9. Bloch, R. J., and D. W. Pumplin. 1992. A model of spectrin as a concertina in the erythrocyte membrane skeleton. Trends Cell Biol. 2: 186-189.
10. Bourett, T. M., and R. J. Howard. 1991. Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163: 199-202.
11. Braun, E. J., and R. J. Howard. 1994a. Adhesion of fungal spores and germlings to host plant surfaces. Protoplasma 181: 202-212.
12. _, and _. 1994b. Adhesion of Cochliobolus heterosporus conidia and germlings to leaves and artificial surfaces. Exp. Mycol. 18: 211-220.
13. Clipson, N. J. W., and D. H. Jennings. 1990. The role of potassium and sodium in generation of osmotic potential of the marine fungus Dendryphiella salina. Mycol. Res. 94: 1017-1022.
14. Corrêa Jr., A., and H. C. Hoch. 1993. Microinjection of urediospore germlings of Uromyces appendiculatus. Exp. Mycol. 17: 253-273.
15. _, and _. 1995. Identification of thigmoresponsive loci for cell differentiation in Uromyces germlings. Protoplasma 186: 34-40.
16. Edidin, M. 1992. Patches, posts and fences: proteins and plasma membrane domains. Trends Cell Biol. 2: 376-380.
17. Enos, A. P., and N. R. Morris. 1990. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60: 1019-1027.
18. Epstein, L., L. Laccetti, R. C. Staples, and H. C. Hoch. 1987. Cell-substratum adhesive protein involved in surface contact responses of the bean rust fungus. Physiol. Mol. Plant Pathol. 30: 373-388.
19. _, _, _, _, and W. A. Hoose. 1985. Extracellular proteins associated with induction of differentiation in bean rust uredospore germlings. Phytopathology 75: 1073-1076.
20. Eshel, D., A. Urrestarazu, S. Vissers, J. C. Jauniaux, J. C. Van Vliet-Reedijk, R. J. Planta, and I. R. Gibbons. 1993. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc. Natl. Acad. Sci. U.S.A. 90: 11172-11176.
21. Fèvre, M., and M. Rougier. 1982. Autoradiographic study of hyphal cell wall synthesis of Saprolegnia. Arch. Microbiol. 131: 212-215.
22. Freytag, S., and K. Mendgen. 1991. Surface carbohydrates and cell wall structure of in vitro-induced uredospore infection structures of Uromyces viciae-fabae before and after treatments with enzymes and alkali. Protoplasma 161: 94-103.
23. Fukui, Y., T. J. Lynch, H. Brzeska, and E. D. Korn. 1989. Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341: 328-331.
24. 2+ gradient in the oomycete Saprolegnia ferax. Eur. J. Cell Biol. 60: 358-365.
25. + channels in the hyphal tip plasma membrane of the oomycete Saprolegnia ferax. J. Cell Sci. 101: 721-730.
26. Gooday,G.W. 1994. Cell Walls. Pp. 43-62. In: The Growing Fungus Eds., N. A. R. Gow, and G. M. Gadd. Chapman and Hall, London.
27. _, and N. A. R. Gow. 1990. Enzymology of tip growth in fungi. Pp. 31-58. In: Tip Growth in Plant and Fungal Cells. Ed., I. B. Heath Academic Press, Toronto and New York.
28. Goodman, S. R., K. E. Krebs, C. F. Whitfield, B. M. Riederer, and I. S. Zagon. 1988. Spectrin and related molecules CRC Critical Rev. Biochem. 23: 171-234.
29. Goodner, B., and R. S. Quatrano. 1993. Fucus embryogenesis: a model to study the establishment of polarity. The Plant Cell 5: 1471-1481.
30. Grove, S. N., and C. E. Bracker. 1970. Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J. Bacterial. 104: 989-1009.
31. _, and J. A. Sweigard. 1980. Cytochalasin A inhibits spore germination and hyphal tip growth in Gilbertella persicaria. Exp. Mycol. 4: 239-250.
32. Harold, F. M. 1990. To shape a cell: an inquiry into the causes of morphogenesis of microorganisms. Microbiol. Rev. 54: 381-431.
33. Harold, R. L., and F. M. Harold. 1986. Ionophores and cytoshalasins modulate branching in Achlya bisexualis. J. Gen. Microbiol. 132: 213-219.
34. Hartwig. J. H., and D. J. Kwiatkowski. 1991. Actin-binding proteins. Curr. Opin. Cell Biol. 3: 87-97.
35. He, Y., and F. Grinnell. 1994. Stress relaxation of fibroblasts activates a cyclic AMP signalling pathway. J. Cell Biol. 126: 457-464.
36. Heath, I.B. 1982. The effect of nocodazole on the growth and ultrastructure of the fungus Saprolegnia ferax. Evidence against a simple mode of action. Pp. 275-311. In: Microtubules in Microorganisms. Eds., P. Cappuccinelli, and N. R. Morris. Marcel Dekker, New York and Basel.
37. _ 1987. Preservation of a labile cortical array of actin filaments in growing hyphal tips of the fungus Saprolegnia ferax. Eur. J. Cell Biol. 44: 10-16.
38. _ 1990. The roles of actin in tip growth of fungi. Int. Rev Cytol. 123: 95-127.
39. _ 1994. The cytoskeleton. Pp. 99-134. In: The Growing Fungus. Eds., N. A. R. Gow, and G. M. Gadd. Chapman and Hall, London.
40. _ 1995. Integration and regulation of hyphal tip growth. Can. J. Bot. 73: 5131-5139.
41. _, and Greenwood, A. D. 1970. The structure and formation of lomasomes J. gen. Microbiol. 62: 129-137.
42. _, and R.L. Harold. 1992. Actin has multiple roles in the formation and architecture of zoospores of the oomycetes, Saprolegniaferax and Achlya bisexualis. J. Cell Sci. 102: 611-627.
43. _, and M. C. Heath. 1978. Microtubules and organelle movements in the rust fungus Uromyces phaseoli var. vignae. Cytobiologie 16: 393-411.
44. _, and _. 1979. Structural studies of the development of infection structures of cowpea rust, Uromyces phaseoli var. vignae. II. Vacuoles. Can. J. Bot. 57: 1830-1837.
45. _, and S. G. W. Kaminskyj. 1989. The organization of tip-growth-related organelles and microtubules revealed by quantitative analysis of freeze-substituted oömycete hyphae J. Cell Sci. 93: 41-52.
46. _, K. Rethoret, A. L. Arsenault, and F. P. Ottensmeyer. 1985. Improved preservation of the form and contents of wall vesicles and the Golgi apparatus in freeze substituted hyphae of Saprolegnia. Protoplasma 128: 81-93.
47. Heidemann, S. R. 1990. Neuronal tip growth. Pp. 285-316. In: Tip Growth in Plant and Fungal Cells. Ed., I. B. Heath. Academic Press, Toronto and New York.
48. _, and R. E. Buxbaum. 1990. Tension as regulator and integrator of axonal growth. Cell Motil. Cytoskel. 17: 6-10.
49. Heslop-Harrison, J., and Y. Heslop-Harrison. 1989. Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J. Cell Sci. 94: 319-325.
50. Hill, T. W., and J. T. Mullins. 1980a. Hyphal tip growth in Achlya. I. Cytoplasmic organization. Can. J. Microbiol. 26: 1132-1140.
51. _, and _. 1980b. Hyphal tip growth in Achlya. II. Subcellular localization of cellulase and associated enzymes. Can. J. Microbiol. 26: 1141-1146.
52. Hoch, H. C., and R. C. Staples. 1983. Visualization of actin in situ by rhodamine-conjugated phalloin in the fungus Uromyces phaseoli. Eur. J. Cell Biol. 32: 52-58.
53. _, _, B. Whitehead, J. Comeau, and E. D. Wolf. 1987. Signalling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235: 1659-1661.
54. Hostetter, M. K. 1994. Interactions of Candida albicans with eukaryotic cells. Amer. Soc. Microbiol. News 60: 370-374.
55. _, E. J. Michael, and C. M. Bendel. 1993. Complement receptors in Candida albicans and other yeasts: structure, function and role in pathogenesis. Pp. 281-289. ln: Dimorphic Fungi in Biology and Medicine. Eds., H. Vanden Bossche, F. C. Odds and D. Kerridge. Plenum Press, New York and London.
56. 2+-dependent polarization of axis establishment in the tip-growing organism, Saprolegniaferax, by gradients of the ionophore A23187. Eur.J. Cell Biol. 67: 356-362.
57. Hynes, R. O. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
58. Ingber, D. E. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104: 613-627.
59. _, S. Karp, G. Plopper, L. Hansen, and D. Mooney. 1993. Mechanochemical transduction across extracellular matrix and through the cytoskeleton. Pp. 61-78. In: Physical forces and the mammalian cell. Ed., J.A. Frangos. Academic Press, Toronto and New York.
60. Jackson, S. L., and I. B. Heath 1990a. Evidence that actin reinforces the extensible hyphal apex of the oomycete Saprolegnia ferax. Protoplasma 157: 144-153.
61. _, and _. 1990b. Visualization of actin arrays in growing hyphae of the fungus Saprolegnia ferax. Protoplasma 154: 66-70.
62. 2+ dependent apex-directed cytoplasmic contractions in hyphae. Protoplasma 170: 46-52.
63. _, and_. 1993a. Roles of calcium ions in hyphal tip growth Microbiol. Rev. 57: 367-382.
64. _, and _. 1993b. UV microirradiation implicates F-actin in reinforcing growing hyphal tips Protoplasma 175: 67-74.
65. _, and _. 1993c. The dynamic behaviour of cytoplasmic F-actin in growing hyphae. Protoplasma 173: 23-34.
66. Johnston, G. C., J. A. Prendergast, and R. A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113: 539-551.
67. Jung, G., Y. Fukui, B. Martin, and J. A. Hammer. 1993. Sequence, expression pattern, intracellular localization pattern and targeted disruption of the Dictyostelium myosin ID heavy chain isoform. J. Biol. Chem. 268: 14981-14990.
68. Kaminskyj, S. G. W., A. Garrill, and I. B. Heath. 1992a. The relation between turgor and tip growth in Saprolegnia ferax: turgor is necessary but not sufficient to explain apical extension rates. Exp. Mycol. 16: 64-75.
69. _, and Hamer, J. E. 1995. Why search for integrin homologs in fungi? Fung. Genetics News. 42A: 91.
70. _, and Heath, I. B. 1992. Age-dependent differential responses of Saprolegnia hyphal tips to a helical growthinducing factor in the agar substitute, gellan. Exp. Mycol. 16: 230-239.
71. _, and _. 1994. A comparison of techniques for localizing actin and tubulin in hyphae of Saprolegnia ferax. J. Histochem. Cytochem. 42: 523-530.
72. _, and _. 1995. Integrin and spectrin homologues, and cytoplasm-wall adhesion in tip growth. J. Cell Sci. 108: 849-856.
73. 4 tests. Physiol. Plant Pathol. 22: 173-179.
74. _, S. L. Jackson, and I. B. Heath. 1992b. Fixation induces differential polarized translocations of organelles in hyphae of Saprolegnia ferax. J. Microsc. 167: 153-168.
75. _, K. S. Yoon, and I. B. Heath. 1989. Cytoskeletal interactions with post-mitotic migrating nuclei in the oyster mushroom fungus, Pleurotus ostreatus: evidence against a force-generating role for astral microtubules. J. Cell Sci. 94: 663-674.
76. Katz, D., and R. F. Rosenberger 1970. A mutation in Aspergillus nidulans producing hyphal walls which lack chitin. Biochim. Biophys. Acta 208: 452-460.
77. Kiss, J. Z., and L. A. Staehelin. 1993. Structural polarity in the Chara rhizoid: a reevaluation. Amer. J. Bot. 80: 273-282.
78. Koch, A. L. 1982. The shape of the hyphal tips of fungi. J. Gen. Microbiol. 128: 947-951.
79. Kropf, D. L. 1992. Establishment and expression of cellular polarity in fucoid zygotes. Microbiol. Rev. 56: 316-339.
80. Kurtz, M. B., I. B. Heath,J. Marrinan, S. Dreikorn, J. Onishi and C. Douglas. 1994. Morphological effects of lipopeptides against Aspergillus fumigatus correlate with activities against (1 ,3)-β-D-glucanase. Antimicrobial Agents and Chemotherapy 38: 1480-1489.
81. Kwon, Y. H., and H. C. Hoch. 1991. Temporal and spatial dynamics of appressorium formation in Uromyces appendiculatus. Exp. Mycol. 15: 116-131.
82. Levina, N. N., R. R. Lew, and I. B. Heath. (1994). Cytoskeletal regulation of ion channel distribution in the tip growing organism Saprolegnia ferax . J. Cell Sci. 107: 127-134.
83. Littlefield, L. J., and M. C. Heath. 1979. Ultrastructure of Rust Fungi. Academic Press, Toronto and New York.
84. Lopez-Franco, R., S. Bartnicki-Garcia, and C. E. Bracker. 1994. Pulsed growth of fungal hyphal tips. Proc. Natl Acad. Sci. U.S.A. 91: 12228-12232.
85. _, R. J. Howard, and C. E. Bracker. 1995 Satellite Spitzenkörper in growing hyphal tips. Protoplasma 188: 85-103.
86. Luard, E. J. 1982. Growth and accumulation of solutes by Phytophthora cinnamomi and other lower fungi in response to changes in external osmotic potential. J. Gen. Microbiol. 128: 2583-2590.
87. Madden, K., C. Costigan, and M. Snyder. 1991. Cell polarity and morphogenesis in Saccharomyces cerevisiae. Trends Cell Biol. 1: 22-29.
88. 1 subunit react with proteins in vertebrates, invertebrates and fungi. J. Cell Biol. 106: 1765-1772.
89. McGoldrick, C. A., Gruver, C. and May, G. S. 1995. myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J. Cell Biol. 106: 1765-1772.
90. McKerracher, L. J., and I. B. Heath. 1986. Fungal nuclear behaviour analyzed by ultraviolet microbeam irradiation. Cell Motil. Cytoskel. 6: 35-47.
91. _, and _. (1987). Cytoplasmic migration and intracellular organelle movements during tip growth of fungal hyphae. Exp. Mycol. 11: 79-100.
92. Meluh, P. B., and M. D. Rose. 1990. KAR3, a kinesinrelated gene required for yeast nuclear fusion. Cell 60, 1029-1041.
93. Meyer, S. L. F., S. G. W. Kaminskyj, and I. B. Heath. 1988. Nuclear migration in a nud mutant of Aspergillus nidulans is inhibited in the presence of a quantitatively normal population of cytoplasmic microtubules. J. Cell Biol. 106: 773-778.
94. Moloshok, T. D., B. T. Terhune, J. S. Lamboy, and H. C. Hoch. 1994. Fractionation of extracellular matrix components from urediospore germlings of Uromyces. Mycologia 86: 787-794.
95. Money, N. P. 1990. Measurement of hyphal turgor. Exp. Mycol. 14: 416-425.
96. _. 1995. Turgor pressure and the mechanics of fungal penetration. Can. J. Bot. 73: S96-S102.
97. _, and F. M. Harold. 1992. Extension growth of the water mold Achlya: interplay of turgor and wall strength. Proc. Natl. Acad. Sci. U.S.A. 89. 4245-4249.
98. _, and _. 1993. Two water molds can grow without measureable turgor pressure. Planta 190, 426-430.
99. Mulholland, J., D. Preuss, A. Moon, A. Wong, D. Drubin, and D. Botstein. 1994. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125: 381-391.
100. Mullins, J. T. 1973. Lateral branch formation and cellulasem production in the water molds. Mycologia 65: 1007-1014.
101. Olmsted, J. B. 1986. Microtubule-associated proteins. Ann. Rev. Cell Biol. 2: 421-57.
102. _. 1991. Non-motor microtubule-associated proteins. Curr. Opin. Cell Biol. 3: 52-58.
103. Picton, J. M., and M. W. Steer. 1982. A model for the mechanism of tip extension in pollen tubes. J. theor. Biol. 98: 15-20.
104. Pickard, B. G. 1994. Contemplating the plasmalemma control centre model. Protoplasma 182: 1-9.
105. Pierson, E.S., and M. Cresti. 1992. Cytoskeleton and cytoplasmic organization of pollen and pollen tubes. Int. Rev. Cytol. 140: 73-125.
106. _, Miller, D. D., Callaham, D. A., Shipley, A. M., Rivers, B. A., Cresti, M. and Hepler, P. K. 1994. Pollen tube growth is coupled to the extracellular calcium flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypotonic media. The Plant Cell 6: 1815-1828.
107. Prosser, J. I. 1990. Comparison of tip growth in prokaryotic and eukaryotic filamentous organisms. Pp. 233-259. In: Tip Growth in Plant and Fungal Cells. Ed., I. B. Heath. Academic Press, Toronto and New York. I
108. Quatrano, R. S., L. Brian. J. Aldridge, and T. Schultz. 1991. Polar axis fixation in Fucus zygotes: components of the cytoskeleton and extracellular matrix. Devel. Suppl. 1: 11-16.
109. Raudaskoski, M., I. Rupes, and S. Timonen. 1991. Immunofluorescence microscopy of the cytoskeleton in filamentous fungi after quick-freezing and low-temperature fixation. Exp. Mycol. 15: 167-173.
110. Reinhardt, M. O. (1892). Das Wachsthum der Pilzhyphen. Jahrb. wiss. Botanik 23: 479-566.
111. Roberson, R. W. 1992. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84, 41-51.
112. _, and M. S. Fuller. 1988. Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma 146: 143-149.
113. _, and M. M. Vargas. 1994. The tubulin cytoskeleton and its sites of nucleation in hyphal tips of Allomyces macrogynus. Protoplasma 182: 19-31.
114. Robertson, N. F., and S. R. H. Rizvi. 1968. Some observations on the water-relations of the hyphae of Neurosporacrassa. Ann. Bot. 32: 279-291.
115. Sanders, L. C., and E. M. Lord. 1992. A dynamic role for the stylar matrix in pollen tube extension. Int. Rev. Cytol. 140: 297-316.
116. _, C. S. Wang, L. L. Walling, and E. M. Lord. 1991. A homolog of the substrate adhesion molecule vitronectin occurs in four species of flowering plants. The Plant Cell 3: 629-635.
117. Sastry, S. K., and A. F. Horwitz. 1993. Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extraand intracellular initiated transmembrane signalling. Curr. Opin. Cell Biol. 5: 819-831.
118. Saunders, P. T., and A. P. J. Trinci. 1979. Determination of tip shape in fungal hyphae. J. Gen. Microbiol. 110: 469-473.
119. Schindler, M., S. Meiners, and D. A. Cheresh. 1989. RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth. J. Cell Biol. 108: 1955-1965.
120. 1, independent of cell shape. Proc. Natl Acad. Sci. U.S.A. 88: 7849-7853.
121. Staves, M. P., R. Wayne, and A. C. Leopold. 1992. Hydrostatic pressure mimics gravitational pressure in characean cells. Protoplasma 168: 141-152.
122. Stossel, T. P. 1993. On the crawling of animal cells. Science 260, 1086-1094.
123. _, C. Chaponnier, R. M. Ezzell, J. H. Hartwig, P. A. Janmey, D. J. Kwiatowski, S. E. Lind, D. B. Smith, F. S. Southwick, H. L. Yin, and K. S. Zaner. 1985. Nonmuscle actin-binding proteins. Ann. Rev. Cell Biol. 1: 353-402.
124. Tang, X., P. K. Hepler, and S. P. Scordilis. 1989. Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide in Nicotiana pollen tubes. J. Cell Sci. 92: 569-574.
125. Terhune, B. T., and H. C. Hoch. 1993. Substrate hydrophobicity and adhesion of Uromyces urediospores and germlings. Exp. Mycol. 17: 241-252.
126. van Tuinen, D., R. Ortega Perez, and G. Turian. 1986. A search for myosin in elongating hyphae of Neurospora crassa. Bot. Helv. 96: 299-302.
127. Vanderkerckhove, J., and K. Vancompernolle. 1992. Structural relationships of actin-binding proteins. Curr. Opin. Cell Biol. 4: 36-42.
128. Wagner, V. T., L. Brian, and R. S. Quatrano. 1992. Role of a vitronectin-like molecule in embryo adhesion of the brown alga, Fucus. Proc. Natl. Acad. Sci. U.S.A. 90: 3644-3648.
129. Wang, N., J. P. Butler, and D. E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-127.
130. Watts, F. Z., D. M. Miller, and E. Orr. (1985). Identification of myosin heavy chain in Saccharomyces cerevisiae. Nature 316: 83-85.
131. Wayne, R., M. P. Staves, and A. C. Leopold. 1992. The contribution of the extracellular matrix to gravisensing in characean cells. J. Cell Sci. 101: 611-623.
132. Wessels, J. G. H. 1988. A steady-state model for apical wall growth in fungi. Acta Bot. Neerl. 37: 3-16.
133. _. 1990. Role of cell wall architecture in fungal tip growth generation. Pp. 1-29 In: Tip Growth in Plant and Fungal Cells. Ed., I. B. Heath. Academic Press, Toronto and New York.
134. _. (1993). Wall growth, protein excretion and morphogenesis in fungi. (Tansley Review No. 45) New Phytol. 23: 397-413.
135. Williams, M. J., P. E. Hughes, T. E. O'Toole, and M. H. Ginsberg. 1994. The inner world of cell adhesion: integrin cytoplasmic domains. Trends Cell Biol. 4: 109-112.
136. Wyatt, S. E., and N. C. Carpita. 1993. The plant cytoskeleton- cell-wall continuum. Trends Cell Biol. 3: 413-417.
137. Wynn, W. K. 1976. Appressorium formation over stomates by the bean rust fungus: response to a surface-contact stimulus. Phytopathology 66: 136-146.
138. Xiang, X., S. M. Beckwith, and N. R. Morris. 1994. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. U.S.A. 91: 2100-2104.
139. Zhou, X.-L., M. A. Stumpf, H. C. Hoch, and C. Kung. 1991. A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces. Science 253: 1415-1417.
140. Zhu, J.-K., J. Shi, U. Singh, S. E. Wyatt, R. A. Bressan, P. M. Hasegawa, and N. C. Carpita. 1993. Enrichment of vitronectin- and fibronectin-like proteins in NaCl-adapted plant cells and evidence for their involvement in plasma membrane-cell wall adhesion. The Plant Journal 3: 637-646.