Mechanisms of hyphal tip growth: Tube dwelling amebae revisited

Fungal Genetics and Biology

Volumn 28, Issue 2, 1999, Pages 79-93

  Heath, I Brent ^a,b   Steinberg, Gero ^a,b  

^a YORK UNIVERSITY   (Canada)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Amebae; Calcium; Cytoskeleton; Hyphae; Tip growth

Indexed keywords

ACTIN;

AMOEBA; APICAL MEMBRANE; CELL WALL; CYTOPLASM; FUNGUS GROWTH; FUNGUS HYPHAE; NONHUMAN; PRIORITY JOURNAL; PSEUDOPODIUM; REVIEW;

EID: 0033388634     PISSN: 10871845     EISSN: None     Source Type: Journal    
DOI: 10.1006/fgbi.1999.1168     Document Type: Review

References (156)

1. Adams A. E. M., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic mutant Saccharomyces cerevisiae. J. Cell Biol. 98:1984;934-945.
2. Akashi T., Kanbe T., Tanaka K. The role of the cytoskeleton in polarized growth of the germ tube in Candida albicans. Microbiology. 140:1994;271-280.
3. Anderson J. M., Soll D. R. Differences in actin localization during bud and hypha formation in the yeast Candida albicans. J. Gen. Microbiol. 132:1986;2035-2047.
4. Ayscough K. R., Stryker J., Pokala N., Sanders M., Crews P., Drubin D. G. 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. 137:1997;399-416.
5. Bachewich C., Heath I. B. Cytoplasmic migrations and vacuolation are associated with growth recovery in hyphae of Saprolegnia, and are dependent on the cytoskeleton. Mycol. Res. 103:1999;849-858.
6. Bachewich C. L., Heath I. B. Differential cytoplasm-plasma membrane-cell wall adhesion patterns and their relationships to hyphal tip growth and organelle motility. Protoplasma. 200:1997;71-86.
7. Bachewich C. L., Heath I. B. Radial F-actin arrays precede new hypha formation in Saprolegnia: Implications for establishing polar growth and regulating tip morphogenesis. J. Cell Sci. 111:1998;2005-2016.
8. Barr D. J. S. Allochytrium expandens rediscovered: Morphology, physiology and zoospore ultrastructure. Mycologia. 78:1986;439-448.
9. Barr D. J. S. Evolution and kingdoms of organisms from the perspective of a mycologist. Mycologia. 84:1992;1-11.
10. Bartnicki-Garcia S. Role of vesicles in apical growth and a new mathematical model of hyphal morphogenesis. Heath I. B. Tip Growth in Plant and Fungal Cells. 1990;211-232 Academic Press, San Diego.
11. Bartnicki-Garcia S., Lippman E. The bursting tendency of hyphal tips of fungi: Presumptive evidence for a delicate balance between wall synthesis and wall lysis in apical growth. J. Gen. Microbiol. 73:1972;487-500.
12. Bendel C. M., Hostetter M. K. Distinct mechanisms of epithelial adhesion for Candida albicans and Candida tropicalis: Identification of the participating ligands and development of inhibitory peptides. J. Clin. Invest. 92:1993;1850-1849.
13. Benkert R., Obermeyer G., Bentrup F.-W. The turgour pressure of growing lily pollen tubes. Protoplasma. 198:1997;1-8.
14. Benzanilla M., Forsberg S. L., Pollard T. D. Identification of a second myosin-II in Schizosaccharomyces pombe: Myp2p is conditionally required for cytokinesis. Mol. Biol. Cell. 8:1997;2693-2705.
15. Bhattacharya D., Medlin L., Wainwright P., Ariztia E., Bibeau C., Stickel S., Sogin M. Algae containing chlorphylls a + c are paraphyletic: Molecular evolutionary analysis of the chromophyta. Evolution. 46:1992;1801-1817.
16. Bourett T. M., Howard R. J. Ultrastructural immunolocalization of actin in a fungus. Protoplasma. 163:1991;199-202.
17. Bray D. Cell Movements. 1992;Garland, New York.
18. Bray D., Vasiliev J. Networks from mutants. Nature. 338:1989;203-204.
19. Bruns T. D., Vilgalys R., Barns S. M., Gonzalez D., Hibbett D. S., Lane D. J., Simon L., Stickel S., Szaro T. M., Weisberg W. G., Sogin M. L. Evolutionary relationships within the fungi: Analyses of nuclear small subunit rRNA sequences. Mol. Phylogenet. Evol. 1:1993;231-241.
20. Burridge K. Are stress fibres contractile. Nature. 294:1981;691-692.
21. Burridge K., Chrzanowska-Wodnicka M. Focal adhesions, contractility and signaling. Annu. Rev. Cell Dev. Biol. 12:1996;463-519.
22. Butt T. M., Heath I. B. The changing distribution of actin and nuclear behavior during the cell cycle of the mite-pathogenic fungus Neozygites sp. Eur. J. Cell Biol. 46:1988;499-505.
23. Cho C. W., Fuller M. S. Observations of the water expulsion vacuole of Phytophthora palmivora. Protoplasma. 149:1989;47-55.
24. Choi E. Y., Jeon K. W. A spectrin-like protein on membranes of Amoeba proteus as studied with monoclonal antibodies. Exp. Cell Res. 185:1989;154-165.
25. Choi E. Y., Jeon K. W. Role of spectrin in Amoeba proteus, as studied by microinjection of anti-spectrin monoclonal antibodies. Exp. Cell Res. 199:1992;174-178.
26. Condeelis J. Life at the leading edge: The formation of cell protrusions. Annu. Rev. Cell Biol. 9:1993;411-444.
27. Corrêa A. Jr., Hoch H. C. Microinjection of urediospore germlings of Uromyces appendiculatus. Exp. Mycol. 17:1993;253-273.
28. Corrêa A., Staples R. C., Hoch H. C. Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma. 194:1996;91-102.
29. Couch J. N. New or little known Chytridiales. Mycologia. 27:1935;160-175.
30. Doyle T., Botstein D. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl. Acad. Sci. USA. 93:1996;3886-3891.
31. Dunphy G. B., Nolan R. A. Morphogenesis of protoplasts of Entomophthora egressa in simplified culture media. Can. J. Bot. 55:1977;3046-3053.
32. Fukui Y. Toward a new concept of cell motility: Cytoskeletal dynamics in amoeboid movement and cell division. Int. Rev. Cytol. 144:1993;85-127.
33. Gale C., Finkel D., Tao N., Meinke M., McClellan M., Olson J., Kendrick K., Hostetter M. Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proc. Natl. Acad. Sci. USA. 93:1996;357-361.
34. 2+ gradient in the oomycete Saprolegnia ferax. Eur. J. Cell Biol. 60:1993;358-365.
35. Gay J. L., Greenwood A. D. Structural aspects of zoospore production in Saprolegnia ferax with particular reference to the cell and vacuolar membranes. Madelin M. F. The Fungus Spore, Colston Papers. 1966;95-110 Butterworths, London.
36. Goldacre R. J. On the mechanism and control of amoeboid movement. Allen R. D., Kamiya N. Primitive Motile Systems in Cell Biology. 1964;237-256 Academic Press, New York and London.
37. Gooday G. W., Gow N. A. R. Enzymology of tip growth in fungi. Heath I. B. Tip Growth in Plant and Fungal Cells. 1990;31-58 Academic Press, San Diego.
38. Goodson H. V., Anderson B. L., Warrick H. M., Pon L. A., Spudich J. A. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): Myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133:1996;1277-1291.
39. Grebecki A. Membrane and cytoskeleton flow in motile cells with emphasis on the contribution of free-living amoebae. Int. Rev. Cytol. 148:1994;37-80.
40. 2+ regulation of hyphal branch induction. Fung. Genet. Biol. 22:1997;127-139.
41. Grove S. N., Bracker C. E. Protoplasmic organization of hyphal tips among fungi: Vesicles and Spitzenkorper. J. Bacteriol. 104:1970;989-1009.
42. Gupta G., Heath I. B. Actin disruption by latrunculin B causes turgor-related changes in tip growth of Saprolegnia hyphae. Fung. Genet. Biol. 21:1997;64-75.
43. Gustafson K., Vercellotti G., Bendel C., Hostetter M. Molecular mimicry in Candida albicans: Role of an integrin analogue in adhesion of the yeast to the human endothelium. J. Clin. Invest. 87:1991;1896-1902.
44. Hahn K., DeBiasso R., Taylor D. L. Patterns of elevated free calcium and calmodulin activation in living cells. Nature. 359:1992;736-738.
45. Harold F. M., Harold R. L., Money N. P. What forces drive cell wall expansion. Can. J. Bot. 73:1995;S379-S383.
46. Harold R. L., Harold F. M. Configuration of actin microfilaments during sporangium development in Achlya bisexualis: Comparison of two staining protocols. Protoplasma. 171:1992;110-116.
47. Harold R. L., Money N. P., Harold F. M. Growth and morphogenesis in Saprolegnia ferax: Is turgor required. Protoplasma. 191:1996;105-114.
48. Heath I. B. Preservation of a labile cortical array of actin filaments in growing hyphal tips of the fungus Saprolegnia ferax. Eur. J. Cell Biol. 44:1987;10-16.
49. Heath I. B. The roles of actin in tip growth of fungi. Int. Rev. Cytol. 123:1990;95-127.
50. Heath I. B. The cytoskeleton in hyphal growth, organelle movements, and mitosis. Wessels J. G. H., Meinhardt F. The Mycota I Growth, Differentiation and Sexuality. 1994;43-65 Springer Verlag, Berlin.
51. Heath I. B. The cytoskeleton. Gow N. A. R., Gadd G. M. The Growing Fungus. 1995a;99-134 Chapman Hall, London.
52. Heath I. B. Integration and regulation of hyphal tip growth. Can. J. Bot. 73:1995b;S131-S139.
53. Heath I. B., Gay J. L., Greenwood A. D. Cell wall formation in the Saprolegniales: Cytoplasmic vesicles underlying developing walls. J. Gen. Microbiol. 65:1971;225-232.
54. Heath I. B., Greenwood A. D. The structure and formation of lomasomes. J. Gen. Microbiol. 62:1970;129-137.
55. Heath I. B., Harold R. L. Actin has multiple roles in the formation and architecture of zoospores of the oomycetes, Saprolegnia ferax and Achlya bisexualis. J. Cell Sci. 102:1992;611-627.
56. Heath I. B., Heath M. C. Structural studies of the development of infection structures of cowpea rust, Uromyces phaseoli var. vignae. II. Vacuoles. Can. J. Bot. 57:1979;1830-1837.
57. Heath I. B., Rethoret K., Arsenault A. L., Ottensmeyer F. P. Improved preservation of the form and contents of wall vesicles and the Golgi apparatus in freeze substituted hyphae of Saprolegnia. Protoplasma. 128:1985;81-93.
58. Heidemann S. R., Buxbaum R. E. Cell crawling: First the motor, now the transmission. J. Cell Biol. 141:1998;1-4.
59. Herr F. B., Heath M. C. The effects of antimicrotubule agents on organelle positioning in the cowpea rust fungus, Uromyces phaseoli var. vignae. Exp. Mycol. 6:1982;15-24.
60. Hoch H. C., Staples R. C. Ultrastructural organization of the nondifferentiated uredospore germling of Uromyces phaseoli variety typica. Mycologia. 75:1983;795-824.
61. Hoch H. C., Staples R. C. The microtubule cytoskeleton in hyphae of Uromyces phaseoli germlings: Its relationship to the region of nucleation and to the F-actin cytoskeleton. Protoplasma. 124:1985;112-122.
62. Hoffmann J., Mendgen K. Endocytosis and membrane turnover in the germ tube of Uromyces fabae. Fung. Genet. Biol. 24:1998;77-85.
63. Holloway S. A., Heath I. B. Morphogenesis and the role of microtubules in synchronous populations of Saprolegnia zoospores. Exp. Mycol. 1:1977a;9-19.
64. Holloway S. A., Heath I. B. An ultrastructural analysis of the changes in organelle arrangement and structure between the various spore types of Saprolegnia. Can. J. Bot. 55:1977b;1328-1339.
65. Hostetter M., Tao N.-J., Gale C., Herman D., McClellan M., Sharp R., Kendrick K. Antigenic and functional conservation of an integrin I-domain in Saccharomyces cerevisiae. Biochem. Mol. Med. 55:1995;122-130.
66. Howard R. J. Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze-substitution. J. Cell Sci. 48:1981;89-103.
67. Howard R. J., Aist J. R. Hyphal tip cell ultrastructure of the fungus Fusarium: Improved preservation by freeze-substitution. J. Ultrastruct. Res. 66:1979;224-234.
68. Humber R. A. The identity of Entomophaga species (Entomophthorales: Entomophthoraceae) attacking Lepidoptera. Mycotaxon. 21:1984;265-272.
69. 2+-dependent polarization of axis establishment in the tip-growing organism, Saprolegnia ferax, by gradients of the ionophore A23187. Eur. J. Cell Biol. 67:1995;356-362.
70. 2+ gradients in hyphae and branches of Saprolegnia ferax. Fung. Genet. Biol. 21:1997;238-251.
71. Isaac P. K. Cytoplasmic streaming in filamentous fungi. Can. J. Bot. 42:1964;787-792.
72. Jackson S. L., Heath I. B. Evidence that actin reinforces the extensible hyphal apex of the oomycete Saprolegnia ferax. Protoplasma. 157:1990a;144-153.
73. Jackson S. L., Heath I. B. Visualization of actin arrays in growing hyphae of the fungus Saprolegnia ferax. Protoplasma. 154:1990b;66-70.
74. 2+ dependent apex-directed cytoplasmic contractions in hyphae. Protoplasma. 170:1992;46-52.
75. Jackson S. L., Heath I. B. The dynamic behavior of cytoplasmic F-actin in growing hyphae. Protoplasma. 173:1993a;23-34.
76. Jackson S. L., Heath I. B. The roles of calcium ions in hyphal tip growth. Microbiol. Rev. 57:1993b;367-382.
77. Jackson S. L., Heath I. B. UV microirradiation implicates F-actin in reinforcing growing hyphal tips. Protoplasma. 175:1993c;67-74.
78. Janmey P. A. Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56:1994;169-191.
79. Jockusch B. M., Bubeck P., Giehl K., Kroemker M., Moschner J., Rothkegel M., Rüdiger M., Schlüter K., Stanke G., Winkler J. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:1995;379-416.
80. Kaminskyj S. G. W., Garrill A., Heath I. B. The relation between turgor and tip growth in Saprolegnia ferax: Turgor is necessary but not sufficient to determine apical extension rates. Exp. Mycol. 16:1992a;64-75.
81. Kaminskyj S. G. W., Heath I. B. Integrin-mediated cytoplasm/wall linkages in Saprolegnia ferax hyphae: Correlation between distribution and tip growth. J. Cell Sci. 108:1995;849-856.
82. Kaminskyj S. G. W., Heath I. B. Studies on Saprolegnia ferax suggest the general importance of the cytoplasm in determining hyphal morphology. Mycologia. 88:1996;20-37.
83. Kaminskyj S. G. W., Jackson S. L., Heath I. B. Fixation induces differential polarized translocations of organelles in hyphae of Saprolegnia ferax. J. Microsc. 167:1992b;153-168.
84. Kamiya N. The motive force of endoplasmic streaming in the ameba. Allen R. D., Kamiya N. Primitive Motile Systems in Cell Biology. 1964;257-278 Academic Press, New York and London.
85. Kamiya N. The mechanism of cytoplasmic movement in a myxomycete plasmodium. Miller P. L. Aspects of Cell Motility. 1968;199-214 Cambridge Univ. Press, Cambridge.
86. Karling J. S. Two new operculate chytrids. Mycologia. 30:1938;302-312.
87. Kitayama C., Sugimoto A., Yamamoto M. Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe. J. Cell Biol. 137:1997;1309-1319.
88. Klotz S., Smith R. A fibronectin receptor in Candida albicans mediates adherence of the fungus to the extracellular matix. J. Infect. Dis. 163:1991;604-610.
89. Kurtz M. B., Heath I. B., Marrinan J., Dreikorn S., Onoshi J., Douglas C. Morphological effects of lipopeptides against Aspergillus fumigatus correlate with activities against (1,3)-β-d-glucan synthase. Antimicrob. Agents Chemother. 38:1994;1480-1489.
90. Lauffenburger D. A., Horwitz A. F. Cell migration: A physically integrated molecular process. Cell. 84:1996;359-369.
91. 2+ and plasma membrane ion channels in hyphal tip growth of Neurospora crassa. J. Cell Sci. 108:1995;3405-3417.
92. Li J., Heath I. B. The behaviour of F-actin during the zoosporic phases of the chytridiomycete gut fungi Neocallimastix and Orpinomyces. Exp. Mycol. 18:1994;57-69.
93. Longcore J. E., Pessier A. P., Nichols D. K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 91:1999;219-227.
94. López-Franco R., Bartnicki-Garcia S., Bracker C. E. Pulsed growth of fungal hyphal tips. Proc. Natl Acad. Sci. USA. 91:1994;12228-12232.
95. López-Franco R., Bracker C. E. Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma. 195:1996;90-111.
96. 1 subunit react with proteins in vertebrates, invertebrates and fungi. J. Cell Biol. 106:1988;1765-1772.
97. May K. M., Watts F. Z., Jones N., Hyams J. S. Type II myosin involved in cytokinesis in the fission yeast, Schizosaccharomyces pombe. Cell Motil. Cytoskel. 38:1997;385-396.
98. May K., Wheatly S., Amin V., Hyams J. The myosin ATPase inhibitor 2,3-butanedione-2-monoxime (BDM) inhibits tip growth and cytokinesis in the fission yeast, Schizosaccharomyces pombe. Cell Motil. Cytoskel. 41:1998;117-125.
99. McDaniel D. P., Roberson R. W. γ-Tubulin is a component of the Spitzenkörper and centrosomes in hyphal-tip cells of Allomyces macrogynus. Protoplasma. 203:1998;118-123.
100. McGoldrick C. A., Gruver C., May G. S. myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J. Cell Biol. 128:1995;577-587.
101. McKerracher L. J., Heath I. B. Polarized cytoplasmic movement and inhibition of saltations induced by calcium-mediated effects of microbeams in fungal hyphae. Cell Motil. Cytoskel. 6:1986;136-145.
102. McKerracher L. J., Heath I. B. Cytoplasmic migration and intracellular organelle movements during tip growth of fungal hyphae. Exp. Mycol. 11:1987;79-100.
103. McLarty D. A. Studies in the family Woroninaceae. I. Discussion of a new species including a consideration of the genera Pseudolpidium and Olpidiopsis. Bull. Torrey Bot. Club. 68:1941;49-66.
104. 2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lillium longiflorum. J. Cell Sci. 110:1997;1269-1278.
105. Mitchison T. J., Cramer L. P. Actin-based cell motility and cell locomotion. Cell. 84:1996;371-379.
106. Money N. P. Wishful thinking of turgor revisited: The mechanics of fungal growth. Fung. Genet. Biol. 21:1997;173-187.
107. Money N. Why oomycetes have not stopped being fungi. Mycol. Res. 102:1998;767-768.
108. Money N. P., Harold F. M. Extension growth of the water mold Achlya: Interplay of turgor and wall strength. Proc. Natl. Acad. Sci. USA. 89:1992;4245-4249.
109. Money N. P., Harold F. M. Two water molds can grow without measurable turgor pressure. Planta. 190:1993;426-430.
110. Money N. P., Hill T. W. Correlation between endoglucanase secretion and cell wall strength in oomycete hyphae: implications for growth and morphogenesis. Mycologia. 89:1997;777-785.
111. Montegi F., Nakano K., Kitayama C., Yamamoto M., Mabuchi I. Identification of Myo3, a second type-II myosin heavy chain in the fission yeast Schizosaccharomyces pombe. FEBS Letts. 420:1997;161-166.
112. Morris N. R., Xiang X., Beckwith S. M. Nuclear migration advances in fungi. Trends. Cell Biol. 5:1995;278-282.
113. Mulholland J. M., Preuss D., Moon A., Wong A., Drubin D., Botstein D. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell. Biol. 125:1994;381-391.
114. Orpin C. G. Studies on the rumen flagellate Neocallimastix frontalis. J. Gen. Microbiol. 91:1975;249-262.
115. Pickett-Heaps J., Klein A. Tip growth in plant cells may be amoeboid and not generated by turgour pressure. Proc. R. Soc. B. 265:1998;1453-1459.
116. Pierson E. S., Miller D. D., Callaham D. A., van Aken J., Hackett G., Hepler P. K. Tip-localized calcium entry fluctuates during pollen tube growth. Dev. Biol. 174:1996;160-173.
117. Pieterse C. M. J., van West P., Verbakel H. M., Brassé P. W. H. M., van den Berg-Velthuis G. C. M., Grovers F. Structure and genomic organization of the ipiB and ipiO gene clusters of Phytophthora infestans. Gene. 138:1994;67-77.
118. Pollard T. D. Purification of a high molecular weight actin filament gelation protein from Acanthamoeba that shares antigenic determinants with vertebrate spectrins. J. Cell Biol. 99:1984;1970-1980.
119. Powell M. J. Spizellomyces (Phlyctochytrium) kneipii. Fuller M. S., Jaworski A. Zoosporic Fungi in Teaching and Research. 1987;303 Southeastern Publishing, Athens.
120. Reinhardt M. O. Das Wachsthum der Pilzhyphen. Jahrb. Wiss. Bot. 23:1892;479-566.
121. Reynaga-Peña C. G., Bartnicki-Garcia S. Apical branching in a temperature sensitive mutant of Aspergillus niger. Fung. Genet. Biol. 22:1997;153-167.
122. Reynaga-Peña C. G., López-Franco R., Bartnicki-Garcia S. Cytoplasmic contractions in fungal hyphae and their morphogenetic consequences. Inoculum. 47:1996;27.
123. Riquelme M., Reynaga-Peña C. G., Gierz G., Bartnicki-García S. What determines growth direction in fungal hyphae. Fung. Genet. Biol. 24:1998;101-109.
124. Roberson R. W. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia. 84:1992;41-51.
125. Roberson R. W., Fuller M. S. Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma. 146:1988;143-149.
126. Roberson R. W., Vargas M. M. The tubulin cytoskeleton and its sites of nucleation in hyphal tips of Allomyces magrogynus. Protoplasma. 182:1994;19-31.
127. Robinow C. F. Observations on cell growth, mitosis, and division in the fungus Basidiobolus ranarum. J. Cell Biol. 17:1963;123-152.
128. Roos U. P., Turian G. Hyphal tip organization in Allomyces arbuscula. Protoplasma. 93:1977;231-247.
129. Runeberg P., Raudaskoski M., Virtanen I. Cytoskeletal elements in the hyphae of the homobasidiomycete Schizophyllum commune visualized with indirect immunofluorescence and NBD-phallacidin. Eur. J. Cell Biol. 41:1986;25-32.
130. Salo V., Niini S. S., Virtanen I., Raudaskoski M. Comparative immunocytochemistry of the cytoskeleton of filamentous fungi with dikaryotic and multinucleate hyphae. J. Cell Sci. 94:1989;11-24.
131. Sepsenwol S., Ris H., Roberts T. M. A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum. J. Cell Biol. 108:1989;55-66.
132. Sparrow F. K. Aquatic Phycomycetes. 1960;University of Michigan Press, Ann Arbor.
133. Srinivasan S., Vargas M. M., Roberson R. W. Functional, organizational, and biochemical analysis of actin in hyphal tip cells of Allomyces macrogynus. Mycologia. 88:1996;57-70.
134. Steele G. C., Trinci A. P. J. The extension zone of mycelial hyphae. New Phytol. 75:1975;583-587.
135. Steinberg G. Organelle transport and molecular motors in fungi. Fung. Genet. Biol. 24:1998;161-177.
136. Steinberg G., McIntosh J. R. Effects of the myosin inhibitor 2,3-butanedione monoxime on the physiology of fission yeast. Eur. J. Cell Biol. 77:1998;284-293.
137. Steinberg G., Schliwa M. Organelle movements in the wild type and wallless fz;sg;os-1 mutants of Neurospora crassa are mediated by cytoplasmic microtubules. J. Cell Sci. 106:1993;555-564.
138. Steinberg G., Schliwa M., Lehmler C., Bölker M., Kahmann R., McIntosh J. R. Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J. Cell Sci. 111:1998;2235-2255.
139. Tang X., Lancelle S. A., Hepler P. K. Fluorescence microscopic localization of actin in pollen tubes: comparison of actin antibody and phalloidin staining. Cell Motil. Cytoskel. 12:1989;216-224.
140. Temperli E., Roos U.-P., Hohl H. R. Actin and tubulin cytoskeletons in germlings of the oomycete fungus Phytophthora infestans. Eur. J. Cell Biol. 53:1990;75-88.
141. glued, the largest subunit of the dynactin complex, is nonessential in Neurospora but required for nuclear distribution. Mol. Biol. Cell. 7:1996;731-742.
142. Torralba S., Raudaskoski M., Pedregosa A. Effects of methyl benzimidazole-2-yl carbamate on microtubulue and actin cytoskeleton in Aspergillus nidulans. Protoplasma. 202:1998a;54-64.
143. Torralba S., Raudaskoski M., Pedregosa A. M., Laborda F. Effect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nudulans. Microbiology. 144:1998;45-53.
144. Trevithick J. R., Galsworthy P. R. Morphology of slime variants of Neurospora crassa growing on a glass surface in liquid medium. 1. Under normal conditions and 2. In the presence of inhibitors. Arch. Microbiol. 115:1977;109-118.
145. Tsukamoto M., Yamamoto M., Tanabe S., Kamada T. Cytochalasin-E-resistant mutants of Coprinus cinereus: Isolation and genetic, biochemical, and cytological analyses. Fung. Genet. Biol. 20:1996;52-58.
146. Tyrrell D. Occurrence of protoplasts in the natural life cycle of Entomophthora egressa. Exp. Mycol. 1:1977;259-263.
147. Tyrrell D., MacLeod D. M. Spontaneous formation of protoplasts by a species of Entomophthora. J. Invert. Pathol. 19:1972;354-360.
148. Waddle J. A., Karpova T. S., Waterston R. H., Cooper J. A. Movement of cortical actin patches in yeasts. J. Cell Biol. 132:1996;861-870.
149. Wainwright P., Hinkle G., Sogin M., Stickel S. Monophyletic origins of the metazoa: and evolutionary link with fungi. Science. 260:1993;340-342.
150. Watts F. Z., Shiels G., Orr E. The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J. 6:1987;3499-3505.
151. Wessels J. G. H. Cell wall synthesis in apical hyphal growth. Int. Rev. Cytol. 104:1986;37-79.
152. Wessels J. G. H. A steady-state model for apical wall growth in fungi. Acta Bot. Neerl. 37:1988;3-16.
153. Wessels J. G. H. Role of cell wall architecture in fungal tip growth generation. Heath I. B. Tip Growth in Plant and Fungal Cells. 1990;1-29 Academic Press, San Diego.
154. Wessels J. G. H., Sietsma J. H., Sonnenberg A. S. M. Wall synthesis and assembly during hyphal morphogenesis in Schizophyllum commune. J. Gen. Microbiol. 129:1983;1607-1616.
155. Wubah D. A., Fuller M. S., Akin D. E. Neocallimastix: A comparative morphological study. Can. J. Bot. 69:1991;835-843.
156. Zopf W. Zur Kenntniss der Phycomyceten. I. Zur Morphologie und Biologie der Ancylisteen und Chytidiaceen. Nova Acta Acad. Leop.-Carl. 47:1884;143-236.