Tip growth in filamentous fungi: A road trip to the apex

Annual Review of Microbiology

Volumn 67, Issue , 2013, Pages 587-609

  Riquelme, Meritxell ^a  

^a CENTRO DE INVESTIGACIÓN CIENTÍFICA Y DE EDUCACIÓN SUPERIOR DE ENSENADA   (Mexico)

Author keywords

Apical growth; Fungal morphogenesis; Hyphae; Polarity

Indexed keywords

FUNGAL RNA; RAB PROTEIN; SNARE PROTEIN;

ARTICLE; CELL EXPANSION; CYTOSKELETON; FUNGAL CELL WALL; FUNGAL SPORE GERMINATION; FUNGUS GROWTH; FUNGUS HYPHAE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SECRETORY PATHWAY; SECRETORY VESICLE; TROPISM;

CELL MEMBRANE; CELL POLARITY; FUNGAL PROTEINS; FUNGI; HYPHAE; SECRETORY VESICLES;

EID: 84884523520     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155652     Document Type: Article

References (184)

1. Abe M, Qadota H, Hirata A, Ohya Y. 2003. Lack of GTP-bound Rho1p in secretory vesicles of Saccharomyces cerevisiae. J. Cell Biol. 162:85-97
2. Abenza JF, Galindo A, Pantazopoulou A, Gil C, de los Rios V, Peñalva MA. 2010. Aspergillus RabBRab5 integrates acquisition of degradative identity with the long distance movement of early endosomes. Mol. Biol. Cell 21:2756-69
3. Abenza JF, Pantazopoulou A, Rodriguez JM, Galindo A, Peñalva MA. 2009. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10:57-75
4. Adams TH, Wieser JK, Yu J-H. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62:35-54
5. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824-27
6. Ang AL, Taguchi T, Francis S, Folsch H, Murrells LJ, et al. 2004. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167:531-43
7. Araujo-Bazan L, Peñalva MA, Espeso EA. 2008. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol. Microbiol. 67:891-905
8. Araujo-Palomares CL, Castro-Longoria E, Riquelme M. 2007. Ontogeny of the Spitzenkörper in germlings of Neurospora crassa. Fungal Genet. Biol. 44:492-503
9. Araujo-Palomares CL, Richthammer C, Seiler S, Castro-Longoria E. 2011. Functional characterization and cellular dynamics of the CDC-42-RAC-CDC-24 module in Neurospora crassa. PLoS One 6:e27148
10. Araujo-Palomares CL, Riquelme M, Castro-Longoria E. 2009. The polarisome component SPA-2 localizes at the apex of Neurospora crassa and partially colocalizes with the Spitzenkörper. Fungal Genet. Biol. 46:551-63
11. Archer DB, Connerton IF, MacKenzie DA. 2008. Filamentous fungi for production of food additives and processing aids. Adv. Biochem. Eng. Biotechnol. 111:99-147
12. Arkowitz RA, Bassilana M. 2011. Polarized growth in fungi: symmetry breaking and hyphal formation. Semin. Cell Dev. Biol. 22:806-15
13. Aronov S, Gelin-Licht R, Zipor G, Haim L, Safran E, Gerst JE. 2007. mRNAs encoding polarity and exocytosis factors are cotransported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:3441-55
14. Aronson JM. 1965. The cell wall. In The Fungi, ed.GCAinsworth, AS Sussman, pp. 49-76. London/New York: Academic
15. Barrowman DB, ReinischK, Ferro-Novick S. 2010.TRAPPcomplexes in membrane traffic: convergence through a common Rab. Nat. Rev. Mol. Cell Biol. 11:759-63
16. Bartnicki-García S. 1968. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu. Rev. Microbiol. 22:87-108
17. Bartnicki-García S. 1973. Fundamental aspects of hyphal morphogenesis. In Microbial Differentiation, ed. JM Ashworth, E Smith, pp. 245-67. Cambridge, UK: Cambridge Univ. Press
18. Bartnicki-García S. 1987. Chitosomes and chitin biogenesis. Food Hydrocolloids 1:353-58
19. Bartnicki-García S. 1990. Role of vesicles in apical growth and a new mathematical model of hyphal morphogenesis. In Tip Growth in Plants and Fungal Cells, ed. IB Heath, pp. 211-32. San Diego, CA: Academic
20. Bartnicki-García S. 2002. Hyphal tip growth: outstanding questions. In Molecular Biology of Fungal Development, ed. HD Osiewacz, pp. 29-58. New York: Marcel Dekker
21. Bartnicki-García S, Bartnicki DD, Gierz G, López-Franco R, Bracker CE. 1995. Evidence that Spitzenkörper behavior determines the shape of a fungal hypha: a test of the hyphoid model. Exp. Mycol. 19:153-59
22. Bartnicki-García S, Bracker CE, Gierz G, López-Franco R, Lu HS. 2000. Mapping the growth of fungal hyphae: orthogonal cell wall expansion during tip growth and the role of turgor. Biophys. J. 79:2382-90
23. Bartnicki-García S, Gierz G. 1993. Mathematical analysis of the cellular basis of fungal dimorphism. In Dimorphic Fungi in Biology and Medicine, ed. H Bossche, F Odds, D Kerridge, pp. 133-44. New York: Springer
24. Bartnicki-García S, Hergert F, Gierz G. 1989. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153:46-57
25. Bartnicki-García S, Lippman E. 1969. Fungal morphogenesis: cell wall construction in Mucor rouxii. Science 165: 302-4
26. Becht P, König J, Feldbr ügge M. 2006. The RNA-binding protein Rrm4 is essential for polarity in Ustilago maydis and shuttles along microtubules. J. Cell Sci. 119:4964-73
27. Becht P, Vollmeister E, Feldbrügge M. 2005. Role for RNA-binding proteins implicated in pathogenic development of Ustilago maydis. Eukaryot. Cell 4:121-33
28. Berepiki A, Lichius A, Read ND. 2011. Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 9:876-87
29. Berepiki A, LichiusA, Shoji JY, Tilsner J, ReadND. 2010. F-actin dynamics in Neurospora crassa. Eukaryot. Cell 9:547-57
30. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153-66
31. Bourett TM, Howard RJ. 1991. Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163:199-202
32. Bowman BJ, Draskovic M, Freitag M, Bowman EJ. 2009. Structure and distribution of organelles and cellular location of calcium transporters in Neurospora crassa. Eukaryot. Cell 8:1845-55
33. Bracker CE, Murphy DJ, Lopez-Franco R. 1997. Laser microbeam manipulation of cell morphogenesis in growing fungal hyphae. Proc. SPIE 2983. doi:10.1117/12.274325
34. Brand A. 2012. Hyphal growth in human fungal pathogens and its role in virulence. Int. J. Microbiol. 2012:517529
35. Brody S. 1973. Metabolism, cell walls, and morphogenesis. In Developmental Regulation: Aspects of Cell Differentiation, ed. S Coward, pp. 107-54. New York: Academic
36. Bruno KS, Aramayo R, Minke PF, Metzenberg RL, Plamann M. 1996. Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J. 15:5772-82
37. Brunswik H. 1924. Untersuchugen uber die Geslechts und Kernverhaltnisse bei der Hymenomyzetengattung Coprinus. Jena, Ger.: Gustav Fisher. 152 pp.
38. Bulawa CE. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47:505-34
39. Butler GM. 1961. Growth of hyphal branching systems in Coprinus disseminatus. Ann. Bot. 25:341-52
40. Cai H, Reinisch K, Ferro-Novick S. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12:671-82
41. Castle E. 1958. The topography of tip growth in a plant cell. J. Gen. Physiol. 41:913-26
42. Chang F, Peter M. 2003. Yeasts make their mark. Nat. Cell Biol. 5:294-99
43. Charles E, Bracker JR-H, Salomon Bartnicki-García. 1976. Structure and transformation of chitin synthetase particles (chitosomes) during microfibril synthesis in vitro. Proc. Natl. Acad. Sci. USA 73:4570-74
44. Choi W-J, Santos B, Duran A, Cabib E. 1994. Are yeast chitin synthases regulated at the transcriptional or the posttranslational level? Mol. Cell. Biol. 14:7685-94
45. Choquer M, Boccara M, Goncalves IR, Soulié MC, Vidal-Cros A. 2004. Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur. J. Biochem. 271:2153-64
46. Crampin H, Finley K, Gerami-Nejad M, Court H, Gale C, et al. 2005. Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae. J. Cell Sci. 118:2935-47
47. Dagdas YF, Yoshino K, Dagdas G, Ryder LS, Bielska E, et al. 2012. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science 336:1590-95
48. Delgado-Alvarez DL, Callejas-Negrete OA, Gómez N, Freitag M, Roberson RW, et al. 2010. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet. Biol. 47:573-86
49. Echauri-Espinosa RO, Callejas-Negrete OA, Roberson RW, Bartnicki-García S, Mouriño-Pérez RR. Coronin is a component of the endocytic collar of hyphae of Neurospora crassa and is necessary for normal growth and morphogenesis. PLoS One 7:e38237
50. Feierbach B, Verde F, Chang F. 2004. Regulation of a formin complex by the microtubule plus end protein tea1p. J. Cell Biol. 165:697-707
51. Finley KR, Berman J. 2005. Microtubules in Candida albicans hyphae drive nuclear dynamics and connect cell cycle progression to morphogenesis. Eukaryot. Cell 4:1697-711
52. Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND. 2000. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 198:246-59
53. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, et al. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-94
54. Fleissner A, Leeder AC, Roca MG, Read ND, Glass NL. 2009. Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc. Natl. Acad. Sci. USA 106:19387-92
55. Fleissner A, Simonin AR, Glass NL. 2008. Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol. Biol. 475:21-38
56. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, et al. 2000. Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J. Biol. Chem. 275:27594-607
57. Gierz G, Bartnicki-García S. 2001. A three-dimensional model of fungal morphogenesis based on the vesicle supply center concept. J. Theor. Biol. 208:151-64
58. Girbardt M. 1957. Der Spitzenkörper Von Polystictus Versicolor (L). Planta 50:47-59
59. Girbardt M. 1969. Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma 67:413-41
60. Gladfelter AS. 2006. Control of filamentous fungal cell shape by septins and formins. Nat. Rev. Microbiol. 4:223-29
61. GlassNL, Rasmussen C, RocaMG, Read ND. 2004. Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol. 12:135-41
62. Gohre V, Vollmeister E, Bolker M, Feldbrugge M. 2012. Microtubule-dependent membrane dynamics in Ustilago maydis: trafficking and function of Rab5a-positive endosomes. Commun. Integr. Biol. 5:485-90
63. GoodayGW. 1971. An autoradiographic study of hyphal growth of some fungi. J. Gen. Microbiol. 67:125-33
64. Gooday GW. 1978. The enzymology of hyphal growth. In Filamentous Fungi, ed. JE Smith, DR Berry, pp. 51-77. London: Arnold
65. Gould GW, Lippincott-Schwartz J. 2009. New roles for endosomes: from vesicular carriers to multipurpose platforms. Nat. Rev. Mol. Cell Biol. 10:287-92
66. Grosshans BL, Andreeva A, Gangar A, Niessen S, Yates JR 3rd, et al. 2006. The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J. Cell Biol. 172:55-66
67. Grove SN, Bracker CE. 1970. Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J. Bacteriol. 104:989-1009
68. Harold FM. 1990. To shape a cell: an inquiry into the causes of morphogenesis of microorganisms. Microbiol. Rev. 54:381-431
69. Harold FM. 1997. How hyphae grow: morphogenesis explained? Protoplasma 197:137-47
70. Harold FM. 2005. Molecules into cells: specifying spatial architecture. Microbiol. Mol. Biol. Rev. 69:544-64
71. Harris SD. 2006. Cell polarity in filamentous fungi: shaping the mold. Int. Rev. Cytol. 251:41-77
72. Harris SD. 2011. Hyphal morphogenesis: an evolutionary perspective. Fungal Biol. 115:475-84
73. Harris SD, Momany M. 2004. Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet. Biol. 41:391-400
74. Harris SD, Read ND, Roberson RW, Shaw BD, Seiler S, et al. 2005. Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryot. Cell 4:225-29
75. Heath IB. 1990. Tip Growth in Plant and Fungal Cells. San Diego, CA: Academic
76. Higashitsuji Y, Herrero S, Takeshita N, Fischer R. 2009. The cell end marker protein TeaC is involved in growth directionality and septation in Aspergillus nidulans. Eukaryot. Cell 8:957-67
77. Hoch HC, Staples RC. 1985. The microtubule cytoskeleton in hyphae of Uromyces phaseoli germlings: its relationship to the region of nucleation and to the F-actin cytoskeleton. Protoplasma 124:112-22
78. Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED. 1987. Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235:1659-62
79. Hochstenbach F, Klis FM, Van DenEndeH, Donselaar EV, Peters PJ, Klausner RD. 1998. Identification of a putative alpha-glucan synthase essential for cell wall construction andmorphogenesis in fission yeast. Proc. Natl. Acad. Sci. USA 95:9161-66
80. Hohmann-Marriott MF, Uchida M, van de Meene AM, Garret M, Hjelm BE, et al. 2006. Application of electron tomography to fungal ultrastructure studies. New Phytol. 172:208-20
81. Horio T, Oakley BR. 2005. The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol. Biol. Cell 16:918-26
82. Howard RJ. 1981. Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze-substitution. J. Cell Sci. 48:89-103
83. Howard RJ, Aist JR. 1980. Cytoplasmic microtubules and fungal morphogenesis: ultrastructural effects of methyl benzimidazole-2-ylcarbamate determined by freeze-substitution of hyphal tip cells. J. Cell Biol. 87:55-64
84. Hsu VW, Bai M, Li J. 2012. Getting active: protein sorting in endocytic recycling. Nat. Rev. Mol. Cell Biol. 13:323-28
85. HunsleyDBJH. 1970. The ultrastructural architecture of thewalls of some hyphal fungi. J. Gen. Microbiol. 62:203-18
86. Inoue SB, Qadota H, Arisawa M, Watanabe T, Ohya Y. 1999. Prenylation of Rho1p is required for activation of yeast 1, 3-glucan synthase. J. Biol. Chem. 274:38119-24
87. Johnson BF. 1968. Lysis of yeast cell walls induced by 2-deoxyglucose at their sites of glucan synthesis. J. Bacteriol. 95:1169-72
88. Jones LA, Sudbery PE. 2010. Spitzenkörper, exocyst, and polarisome components in Candida albicans hyphae show different patterns of localization and have distinct dynamic properties. Eukaryot. Cell 9:1455-65
89. Justa-Schuch D, Heilig Y, Richthammer C, Seiler S. 2010. Septum formation is regulated by the RHO4- specific exchange factors BUD3 and RGF3 and by the landmark protein BUD4 in Neurospora crassa. Mol. Microbiol. 76(1):220-35
90. Kaminsky SGW, Hamer JE. 1998. hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans. Genetics 148:669-80
91. Knechtle P, Dietrich F, Philippsen P. 2003. Maximal polar growth potential depends on the polarisome component AgSpa2 in the filamentous fungus Ashbya gossypii. Mol. Biol. Cell 14:4140-54
92. Koepke J, Kaffarnik F, Haag C, Zarnack K, LuscombeNM, et al. 2011. The RNA-binding protein Rrm4 is essential for efficient secretion of endochitinase Cts1. Mol. Cell. Proteomics 10:M111.011213
93. KohliM, Galati V, Boudier K, Roberson RW, Philippsen P. 2008. Growth-speed-correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. J. Cell Sci. 121:3878-89
94. Latgé JP. 2007. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66:279-90
95. Latgeí JP, Calderone R. 2006. The fungal cell wall. In The Mycota, ed. U Kues, R Fischer, pp. 73-104. Berlin/Heidelberg: Springer
96. Lenardon MD, Milne SA, Mora-Montes HM, Kaffarnik FA, Peck SC, et al. 2010. Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. J. Cell Sci. 123:2199-206
97. Lesage G, SdicuAM, MénardP, Shapiro B, Hussein S, BusseyH. 2004. Analysis of α-1, 3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 167:35-49
98. Lew RR. 2011. How does a hypha grow? The biophysics of pressurized growth in fungi. Nat. Rev. Microbiol. 9:509-18
99. Lichius A, Berepiki A, ReadND. 2011. Form follows function-the versatile fungal cytoskeleton. Fungal Biol. 115:518-40
100. Lichius A, Yáñez-Gutiérrez ME, Read ND, Castro-Longoria E. 2012. Comparative live-cell imaging analyses of SPA-2, BUD-6 and BNI-1 in Neurospora crassa reveal novel features of the filamentous fungal polarisome. PLoS One 7:e30372
101. López-Franco RB, Bracker CE. 1996. Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195:90-111
102. Marchant R, Smith DG. 1968. A serological investigation of hyphal growth in Fusarium culmorum. Arch. Mikrobiol. 63:85-94
103. Martinez-NuñezL, RiquelmeM. 2012. Localization of the (1-3) endoglucanasesEGLC-1andEGLC- 2 and their role in the morphogenesis of Neurospora crassa. Presented at Neurospora 2012, March 8-11. Pacific Grove, CA. 8 pp.
104. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5:121-32
105. McClureWK, Park D, Robinson PM. 1968. Apical organization in the somatic hyphae of fungi. J. Gen. Microbiol. 50:177-82
106. McDaniel DP, Roberson RW. 2000. Microtubules are required for motility and positioning of vesicles and mitochondria in hyphal tip cells of Allomyces macrogynus. Fungal Genet. Biol. 31:233-44
107. 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. 128:577-87
108. Momany M. 2002. Polarity in filamentous fungi: establishment, maintenance and new axes. Curr. Opin. Microbiol. 5:580-85
109. Momany M, Westfall PJ, Abramowsky G. 1999. Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics 151:557-67
110. Money NP. 1995. Turgor pressure and the mechanics of fungal penetration. Can. J. Bot. 73:96-102
111. Money NP. 2011. Introduction: the 200th anniversary of the hypha. Fungal Biol. 115:443-45
112. Morris NR. 1975. Mitotic mutants of Aspergillus nidulans. Genet. Res. 26:237-54
113. Mouriño-Pérez RR, Roberson RW, Bartnicki-García S. 2006. Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet. Biol. 43:389-400
114. Nicolau DV, Mocanasu RC, Livingston PJ, Hanson KL, Nicolau DV. 2005. Laser-based manipulation of growth direction and intracellular processes in fungal hyphae. Proc. SPIE 6036:60360F-F-8
115. Oakley BR, Oakley CO, Yoon Y, Jung MK. 1990. γ-Tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61:1289-301
116. Olsen L, Choffnes ER, Relman DA, Pray L, eds. 2011. Fungal Diseases: An Emerging Threat to Human, Animal, and Plant Health.Washington, DC: Natl. Acad. Press. 488 pp.
117. Pan F, Malmberg RL, MomanyM. 2007. Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol. Biol. 7:103
118. Pantazopoulou A, PeñalvaMA. 2011. Characterization of Aspergillus nidulans RabC/Rab6. Traffic 12:386-406
119. Peñalva MA. 2010. Endocytosis in filamentous fungi: Cinderella gets her reward. Curr. Opin. Microbiol. 13:684-92
120. Plamann M, Minke PE, Tinsley JH, Bruno KS. 1994. Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127:139-49
121. Prosser JI. 1979. Mathematical modelling of mycelial growth. In Fungal Walls and Hyphal Growth, ed. JH Burnett, APJ Trinci, pp. 359-84. Cambridge, UK: Cambridge Univ. Press
122. Reinhardt MO. 1892. DasWachsthum der Pilzhyphen. Jahrb. Wissenschafliche Bot. 23:479-566
123. Reynaga-Peña CG, Gierz G, Bartnicki-García S. 1997. Analysis of the role of the Spitzenkörper in fungal morphogenesis by computer simulation of apical branching in Aspergillus niger. Proc. Natl. Acad. Sci. USA 94:9096-101
124. Riquelme M, Bartnicki-García S. 2004. Key differences between lateral and apical branching in hyphae of Neurospora crassa. Fungal Genet. Biol. 41:842-51
125. Riquelme M, Bartnicki-García S. 2008. Advances in understanding hyphal morphogenesis: ontogeny, phylogeny and cellular localization of chitin synthases. Fungal Biol. Rev. 22:56-70
126. Riquelme M, Bartnicki-García S, González-Prieto JM, Sánchez-León E, Verdín-Ramos JA, et al. 2007. Spitzenkörper localization and intracellular traffic of green fluorescent protein-labeled CHS-3 and CHS- 6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot. Cell 6:1853-64
127. RiquelmeM, Fischer R, Bartnicki-García S. 2003. Apical growth and mitosis are independent processes in Aspergillus nidulans. Protoplasma 222:211-15
128. Riquelme M, Gierz G, Bartnicki-García S. 2000. Dynein and dynactin deficiencies affect the formation and function of the Spitzenkörper and distort hyphal morphogenesis of Neurospora crassa. Microbiology 146:1743-52
129. RiquelmeM, Reynaga-Peña CG, Gierz G, Bartnicki-García S. 1998. What determines growth direction in fungal hyphae? Fungal Genet. Biol. 24:101-9
130. RiquelmeM, Roberson RW, McDanielDP, Bartnicki-García S. 2002. The effects of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa. Fungal Genet. Biol. 37:171-79
131. Rizzoli SO, Jahn R. 2007. Kiss-and-run, collapse and 'readily retrievable' vesicles. Traffic 8:1137-44
132. Roberson RW, Vargas MM. 1994. The tubulin cytoskeleton and its sites of nucleation in hyphal tips of Allomyces macrogynus. Protoplasma 182:19-31
133. Robertson NF. 1965. The fungal hypha. Trans. Br. Mycol. Soc. 48:1-8
134. Rokem JS. 2007. Industrial mycology. In Biotechnology, ed. HW Doelle, EJ DaSilva, ch. 5.10. Oxford, UK: Encyclopedia of Life Support Systems (EOLSS). http://www.eolss.net/
135. Roncero C. 2002. The genetic complexity of chitin synthesis in fungi. Curr. Genet. 41:367-78
136. Ruiz-Herrera J, Bartnicki-García S. 1974. Synthesis of cell wall microfibrils in vitro by a "soluble" chitin synthetase from Mucor rouxii. Science 186:357-59
137. Sánchez-León E, Verdín J, Freitag M, Roberson RW, Bartnicki-García S, Riquelme M. 2011. Traffic of chitin synthase 1 (CHS-1) to the Spitzenkörper and developing septa in hyphae of Neurospora crassa: actin dependence and evidence of distinct microvesicle populations. Eukaryot. Cell 10:683-95
138. Schmitz HP, Kaufmann A, Kohli M, Laissue PP, Philippsen P. 2006. From function to shape: a novel role of a formin in morphogenesis of the fungus Ashbya gossypii. Mol. Biol. Cell 17:130-45
139. Schuchardt I, Assmann D, Thines E, SchuberthC, Steinberg G. 2005. Myosin-V, kinesin-1, and kinesin- 3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol. Biol. Cell 16:5191-201
140. Seiler S, Nargang FE, Steinberg G, Schliwa M. 1997. Kinesin is essential for cell morphogenesis and polarized secretion in Neurospora crassa. EMBO J. 16:3025-34
141. Seiler S, Plamann M. 2003. The genetic basis of cellular morphogenesis in the filamentous fungus Neurospora crassa. Mol. Biol. Cell 14:4352-64
142. Selvaggini S, Munro CA, Paschoud S, Sanglard D, Gow NAR. 2004. Independent regulation of chitin synthase and chitinase activity in Candida albicans and Saccharomyces cerevisiae. Microbiology 150:921-28
143. Sharpless KE, Harris SD. 2002. Functional characterization and localization of the Aspergillus nidulans formin SEPA. Mol. Biol. Cell 13:469-79
144. Shaw BD, Chung DW, Wang CL, Quintanilla LA, Upadhyay S. 2011. A role for endocytic recycling in hyphal growth. Fungal Biol. 115:541-46
145. Sietsma JH, Wessels JGH. 2006. Apical wall biogenesis. In TheMycota, ed.UKues, R Fischer, pp. 53-72. Berlin/Heidelberg: Springer
146. Steinberg G. 2007. On the move: endosomes in fungal growth and pathogenicity. Nat. Rev. Microbiol. 5:309-16
147. Steinberg G. 2007. Tracks for traffic: microtubules in the plant pathogen Ustilago maydis. New Phytol. 174:721-33
148. Steinberg G, Schuster M. 2011. The dynamic fungal cell. Fungal Biol. Rev. 25:14-37
149. Sudbery P. 2011. Fluorescent proteins illuminate the structure and function of the hyphal tip apparatus. Fungal Genet. Biol. 48:849-57
150. Sudbery P, Court H. 2007. Polarised growth in fungi. In Biology of the Fungal Cell, ed. R Howard, NR Gow, pp. 137-66. Berlin/Heidelberg: Springer
151. Sudbery PE. 2001. The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol. Microbiol. 41:19-31
152. Taheri-Talesh N, Horio T, Araujo-Bazan L, Dou X, Espeso EA, et al. 2008. The tip growth apparatus of Aspergillus nidulans. Mol. Biol. Cell 19:1439-49
153. Taheri-Talesh N, Xiong Y, Oakley BR. 2012. The functions of myosin II and myosin V homologs in tip growth and septation in Aspergillus nidulans. PLoS One 7:e31218
154. Takaya N, Yamazaki D, Horiuchi H, Ohta A, Takagi M. 1998. Cloning and characterization of a chitinase-encoding gene (chiA) from Aspergillus nidulans, disruption of which decreases germination frequency and hyphal growth. Biosci. Biotechnol. Biochem. 62:60-65
155. Takeshita N, Fischer R. 2011. On the role of microtubules, cell end markers, and septal microtubule organizing centres on site selection for polar growth in Aspergillus nidulans. Fungal Biol. 115:506-17
156. Takeshita N, Ohta A, Horiuchi H. 2005. CsmA, a class V chitin synthase with a myosin motor-like domain, is localized through direct interaction with the actin cytoskeleton in Aspergillus nidulans. Mol. Biol. Cell 16:1961-70
157. TerBush DR, Maurice T, Roth D, Novick P. 1996. The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15:6483-94
158. Tey WK, North AJ, Reyes JL, Lu YF, Jedd G. 2005. Polarized gene expression determines woronin body formation at the leading edge of the fungal colony. Mol. Biol. Cell 16:2651-59
159. TimberlakeWE. 1991. Molecular genetics of Aspergillus development. Annu. Rev. Genet. 24:5-36
160. Torralba S, Heath IB. 2002. Analysis of three separate probes suggests the absence of endocytosis in Neurospora crassa hyphae. Fungal Genet. Biol. 37:221-32
161. Treitschke S, Doehlemann G, Schuster M, Steinberg G. 2010. The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 22:2476-94
162. Trilla JA, Cos T, Duran A, Roncero C. 1997. Characterization of CHS4 (CAL2), a gene of Saccharomyces cerevisiae involved in chitin biosynthesis and allelic to SKT5 and CSD4. Yeast 13:795-807
163. Trinci APJ, Collinge AJ. 1975. Hyphal wall growth in Neurospora crassa and Geotrichum candidum. J. Gen. Microbiol. 91:355-61
164. Upadhyay S, Shaw BD. 2008. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol. Microbiol. 68:690-705
165. Verdín J, Bartnicki-Garcá́ S, Riquelme M. 2009. Functional stratification of the Spitzenkörper of Neurospora crassa. Mol. Microbiol. 74:1044-53
166. Virag A, Griffiths AJF. 2004. A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet. Biol. 41:213-25
167. Virag A, Harris SD. 2006. Functional characterization of Aspergillus nidulans homologues of Saccharomyces cerevisiae Spa2 and Bud6. Eukaryot. Cell 5:881-95
168. Virag A, LeeMP, Si H, Harris SD. 2007. Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol. Microbiol. 66:1579-96
169. Vollmeister E, Schipper K, Feldbr ügge M. 2012. Microtubule- dependentmRNA transport in the model microorganism Ustilago maydis. RNA Biol. 9:261-68
170. Walworth NC, Brennwald P, Kabcenell AK, Garrett M, Novick P. 1992. Hydrolysis of GTP by Sec4 protein plays an important role in vesicular transport and is stimulated by a GTPase-activating protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2017-28
171. Weber I, Assmann D, Thines E, Steinberg G. 2006. Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 18:225-42
172. Weber I, Gruber C, Steinberg G. 2003. A class-V myosin required for mating, hyphal growth, and pathogenicity in the dimorphic plant pathogen Ustilago maydis. Plant Cell 15:2826-42
173. Wedlich-Söldner R, Bölker M, Kahmann R, Steinberg G. 2000. A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19:1974-86
174. Wedlich-Söldner R, Schulz I, Straube A, Steinberg G. 2002. Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis. Mol. Biol. Cell 13:965-77
175. Wendland Jr, Walther A. 2005. Tip growth and endocytosis in fungi. Plant Cell Monogr. 1:293-310
176. Wessels JGH. 1986. Cell wall synthesis in apical hyphal growth. Int. Rev. Cytol. 104:37-79
177. Westfall PJ, MomanyM. 2002. Aspergillus nidulans septin AspB plays pre- and postmitotic roles in septum, branch, and conidiophore development. Mol. Biol. Cell 13:110-18
178. Whyte JRC, Munro S. 2002. Vesicle tethering complexes in membrane traffic. J. Cell Sci. 115:2627-37
179. Willdenow CL. 1810. Grundiss der Kräuterkunde, zu Vorselungen entworfen. In Foundations of Herb Science Drafted as Lectures. Berlin: Haude und Spener. 638 pp.
180. Wright GD, Arlt J, Poon WC, ReadND. 2007. Optical tweezer micromanipulation of filamentous fungi. Fungal Genet. Biol. 44:1-13
181. Yamamoto A, Hiraoka Y. 2003. Cytoplasmic dynein in fungi: insights from nuclear migration. J. Cell Sci. 116:4501-12
182. YamazakiH, Tanaka A, Kaneko J, Ohta A, HoriuchiH. 2008. Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet. Biol. 45:963-72
183. Zarnack K, Feldbr ügge M. 2007. mRNA trafficking in fungi. Mol. Genet. Genomics 278:347-59
184. Zekert N, Fischer R. 2009. The Aspergillus nidulans kinesin-3 UncA motor moves vesicles along a subpopulation of microtubules. Mol. Biol. Cell 20:673-84