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Chapter 2 : Hyphal Structure

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Abstract:

The ability to understand cytoplasmic structure can provide powerful insights into the biology of cells and organisms. This chapter has briefly reviewed the diversity of hyphal structures and presented examples of how bioimaging has contributed to a broader understanding of hyphal biology and phylogenetic relationships between fungal taxa. At the heart of polarized growth is the secretory pathway in which vesicles are targeted to sites of growth and subsequently fuse with the plasma membrane. In mature hyphae of the septate fungi, these events have given rise to the Spitzenkörper, a complex and dynamic structure that clearly influences hyphal growth and morphogenesis. The presence or absence of certain morphological characters (e.g., septa and Woronin bodies) already has been useful in defining higher taxa, especially since evolutionary polarity often can be established using stable phylogenetic trees based on DNA sequences. Ever-enlarging molecular databases, especially those of whole genomes, are allowing us to look for the genetic basis of many structural features, such as the presence or absence of Woronin body matrix proteins. This capability will allow us to understand the basis of these features not only in an evolutionary sense but also in a functional one. Collaboration among different types of fungal biologists including systematists is essential to understanding structure and how it applies to the study of the Fungi.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2

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Plasma Membrane
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Spindle Pole Bodies
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Smooth Endoplasmic Reticulum
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Cell Wall Biosynthesis
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Figures

Image of FIGURE 1
FIGURE 1

Cytoplasmic order of hyphal tip. (a) Phase-contrast light micrograph of with Spitzenkörper (white arrow), mitochondria (arrowheads), and nucleus (asterisk). Scale bar, 4 μm. (b) Near-median TEM section through cryofixed hypha illustrating Spitzenkörper (white arrow), mitochondria (white arrowheads), rough ER (black arrowheads), vacuoles (black arrows), and nucleus (asterisk). Scale bar, 2 μm. Reprinted from ( ) with permission from the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 2
FIGURE 2

Phase-contrast light micrograph of hyphal tip illustrating the phase-dark region (arrow) and the subtending phase-light core of Spitzenkörper. Mitochondria are indicated by arrowheads. Scale bar, 1.5 μm.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 3
FIGURE 3

Near-median TEM section through hyphal tip of (Ascomycota) illustrating structural components of the Spitzenkörper and surrounding cytoplasm. Shown are apical vesicles (white arrows); microvesicles (white arrowheads); central core (asterisk); MTs (black arrows); MFs (small white arrows); plasma membrane at sites of exocytosis (black arrowheads); ribosomes (small black arrows); cell wall (CW); cell wall inclusions (black asterisks). Scale bar, 200 nm.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 4
FIGURE 4

Phase-contrast light micrograph of hyphal tip illustrating phase-light core of Spitzenkörper subtended by mitochondria (asterisk). Scale bar, 4 μm. Reprinted from ( ) with permission from the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 5
FIGURE 5

Near-median TEM section through hyphal tip of illustrating structural components of the Spitzenkörper and surrounding cytoplasm: central core (asterisk); microvesicles (small arrows); MTs (arrows); and mitochondria (arrowheads). Scale bar, 1.7 μm. Reprinted from ( ) with permission from the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 6
FIGURE 6

TEM of nuclei of illustrating prominent nucleolus (asterisk), nuclear pore complexes (white arrowheads), SPB (white arrow), mitochondrion (m), rough ER (black arrows), and vacuole (V). Scale bar, 350 nm.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 7
FIGURE 7

TEM of SPB and mitosis. (a and b) Sections 3 and 5 of a complete series of 6 through a longitudinally sectioned late interphase SPB of showing the disk form (arrowheads) of the SPB characteristic of Ascomycota and Pucciniomycotina, Basidiomycota. Shown are the middle piece of SPB (white arrows), nuclear envelope (black arrow), and the nucleus (N). Scale bar, 0.2 μm. Reprinted from the ( ) with permission of the publisher. (c and d) Sections 3 and 4 of a complete series of 8 through a late prophase SPB of (Agaricomycotina, Basidiomycota) showing the two globular elements (asterisks) and middle piece (white arrows) surrounded by a ribosome-free zone; an intranuclear element (black arrowhead) consisting of two layers lies within the nucleus (N) adjacent to the nuclear envelope. The intranuclear element is characteristic of many members of Ascomycota and Basidiomycota. Scale bar, 0.2 μm. Reprinted from the (Lu and McLaughlin, 1995) with permission of the publisher. (e) The metaphase SPB of is a disk (asterisk) set in a pore in the nuclear envelope surrounded by a membranous cap (MC). S, spindle. Scale bar, 0.2 μm. Reprinted from the ( ) with permission of the publisher. (f) The metaphase SPB of (Agaricomycotina, Basidiomycota) is a globular element (G) with a dense inclusion lying in a large polar fenestra (delimited by arrows) and a mostly continuous nuclear envelope with a few gaps (arrowhead). Scale bar, 0.5 μm. Reprinted from ( ) with permission of the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 8
FIGURE 8

Differential interference contrast LM of illustrating saltatory motility of a mitochondrion (arrowhead) presented over a 1.5-s period. The Spitzenkörper is indicated by an asterisk. Bar, 5 μm. Reprinted from ( ) with permission from the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 9
FIGURE 9

Elements of the endomembrane system and organelles viewed with TEM. (a) hyphal region III showing vacuoles (V), inflated cisternae of Golgi apparatus (white arrows), rough ER (arrowheads), MVBs (black arrows), and mitochondria (M). Bar, 1.0 μm. Reprinted from (Roberson and Fuller, 2000) with permission from the publisher. (b through e) Serial cross sections through Golgi equivalent of showing apical vesicle (arrowheads), MT (arrows), and a mitochondrion (M). Bar, 0.1 μm. (f) Filasome (arrow) in cortex of hypha. Bar, 0.12 μm. (g) MVB (arrowhead) juxtaposed to MT (arrow) in . Bar, 0.1 μm. From Roberson and Fuller (1988), reproduced with permission from Springer. (h) Flattened vacuolar cisternae (arrows). White arrowheads indicate coated surfaces of vacuoles. Hypha is cut in cross section. Scale bar, 0.2 μm. (i) High magnification of panel h showing coated surfaces of vacuole (black arrow) and cross section of two closely associated MTs (white arrows). Scale bar, 75 nm.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 10
FIGURE 10

Immunofluorescence of MTs in hyphal cells of visualized with confocal microscopy. (a) Reconstruction of six longitudinal optical sections through hypha. MTs are primarily oriented parallel to the growing hyphal axis exhibiting helical curvatures forming a loosely braided meshwork. (b through g) Optical serial sections. MTs are in close proximity to Spitzenkörper but at the time of cell fixation were not traversing Spitzenkörper (asterisk in panel e). MT bundles are indicated by arrows. Scale bar, 3 μm.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 11
FIGURE 11

Immunofluorescence of actin in hyphal cells of visualized with wide-field epifluorescence microscopy. Actin is localized as cortical patches in high numbers beneath apical domes (arrowheads). Actin spot was not observed at the apex (arrow) in these cells. Scale bar, 7 μm. Reprinted from ( ) reproduced with permission from the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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Image of FIGURE 12
FIGURE 12

TEM of septal pore complexes. (a) Simple septal pore in a conidiation mutant of (Ascomycota). Woronin bodies are bound by a single-unit membrane (arrow). Note one of the Woronin bodies (asterisk) plugging the septal pore and the density difference between the cellular compartments above (apical) and below (distal) the cross wall. Scale bar, 300 nm. Courtesy of Beth Richardson and Tony Glenn. (b) Dolipore septal pore and septal pore cap (i.e., parenthosomes) (arrows) of (Basidiomycota) with the cap extending along the cross wall (arrowheads). Scale bar, 125 nm. Reprinted from ( ) with permission of the publisher.

Citation: Roberson R, Abril M, Blackwell M, Letcher P, McLaughlin D, Mouri ÑO-PÉrez R, Riquelme M, Uchida M. 2010. Hyphal Structure, p 8-24. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch2
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References

/content/book/10.1128/9781555816636.ch02
1. Abenza, J. F.,, A. Pantazopoulou,, J. M. Rodríguez,, A. Galindo, and, M. A. Peñalva. 2009. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10:5775.
2. AFTOL. 2007. Assembling the Fungal Tree of Life: Structural and Biochemical Database. University of Minnesota, St. Paul. http://aftol.umn.edu/.
3. Aist, J. R., and, N. R. Morris. 1999. Mitosis in filamentous fungi: how we got where we are. Fungal Genet. Biol. 27:125.
4. Araujo-Bazán, L.,, M. A. Peñalva, and, E. A. Espeso. 2008. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol. Microbiol. 67:891905.
5. Araujo-Palomares, C. L.,, E. Castro-Longoria, and, M. Riquelme. 2007. Ontogeny of the Spitzenkörper in germlings of Neurospora crassa. Fungal Genet. Biol. 44:492503.
6. Ashford, A. E., and, W. G. Allaway. 2007. Motile tubular vacuole systems, p. 49–86. In R. J. Howard and, N. A. R. Gow (ed.), The Mycota: Biology of the Fungal Cell, 2nd ed. Springer-Verlag, Berlin, Germany.
7. Bartnicki-García, S.,, C. E. Bracker,, E. Reyes, and, J. Ruiz-Herrera. 1978. Isolation of chitosomes from taxonomically diverse fungi and synthesis of chitin microfibrils in vitro. Exp. Mycol. 2:173192.
8. Bartnicki-García, S.,, F. Hergert, and, G. Gierz. 1989. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal tip growth. Protoplasma 153:4657.
9. Blackwell, M. 1994. Minute mycological mysteries: the influence of arthropods on the lives of fungi. Mycologia 86:117.
10. Bourett, T. M., and, D. J. McLaughlin. 1986. Mitosis and septum formation in the basidiomycete Helicobasidium mompa. Can. J. Bot. 64:130145.
11. Bourett, T. M., and, R. J. Howard. 1991. Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163:199202.
12. Bourett, T. M.,, S. W. James, and, R. J. Howard. 2007. The endomembrane system in the fungal cell, p. 1–48. In R. J. Howard and, N. A. R. Gow (ed.), The Mycota: Biology of the Fungal Cell, 2nd ed. Springer-Verlag, Berlin, Germany.
13. Bracker, C. E. 1967. Ultrastructure of fungi. Annu. Rev. Phytopathol. 5:343374.
14. Celio, G. J.,, M. Padamsee,, B. T. M. Dentinger,, R. Bauer, and, D. J. McLaughlin. 2006. Assembling the fungal tree of life: constructing the Structural and Biochemical Database. Mycologia 98:850859.
15. Celio, G. J.,, M. Padamsee,, B. T. M. Dentinger,, K. A. Josephsen,, T. S. Jenkinson,, E. G. McLaughlin, and, D. J. McLaughlin. 2007. Septal pore apparatus and nuclear division of Auriscalpium vulgare. Mycologia 99:644654.
16. Chandler, D. E., and, R. W. Roberson. 2009. Current Concepts in Light and Electron Microscopy. Jones and Bartlett Publishing, Boston, MA.
17. Crampin, H.,, K. Finley,, M. Gerami-Nejad,, H. Court,, C. Gale,, J. Berman, and, P. Sudbery. 2005. Candida albicans hyphae have a Spitzenkörper that is distinct from polarisoma found in yeast and pseudohyphae. J. Cell Biol. 118:29352947.
18. Fischer, R. 2007. The cytoskeleton and polarized growth of filamentous fungi, p. 121–135. In R. J. Howard and, N. A. R. Gow (ed.), The Mycota. VIII. Biology of the Fungal Cell, 2nd ed. Springer-Verlag, Berlin, Germany.
19. Fischer-Parton, S.,, R. M. Parton,, P. C. Hickey,, J. Dijksterhuis,, H. A. Atkinson, and, N. D. Read. 2000. Confocal microscopy of FM 4-64 as a tool for analyzing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 198:246259.
20. Freitag, M.,, P. C. Hickey,, N. B. Raju,, E. U. Selker, and, N. D. Read. 2004. GFP as a tool to analyze the organization, dynamics, and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41:897910.
21. Fuchs, F., and, B. Westermann. 2005. Role of unc104/KIF1-related motor proteins in mitochondrial transport in Neurospora crassa. Mol. Biol. Cell 16:153161.
22. Garvalov, B. K.,, B. Zuber,, C. Bouchet-Marquis,, M. Kudryashev,, M. Gruska,, M. Beck,, A. Leis,, F. Frischknecht,, F. Bradke,, W. Baumeister,, J. Dubochet, and, M. Cyrklaff. 2006. Luminal particles within cellular microtubules. J. Cell Biol. 174:759765.
23. Girbardt, M. 1957. Der Spitzenkörper von Polystictus versicolor. Planta 50:4759.
24. Girbardt, M. 1969. Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma 67:413411.
25. Grove, S. N., and, C. E. Bracker. 1970. Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J. Bacteriol. 104:9891009.
26. Harris, S. D.,, N. D. Read,, R. W. Roberson,, B. Shaw,, S. Seiler,, M. Plamann, and, M. Momany. 2004. Spitzenkörper meets polarisome: microscopy, genetics, and genomics converge. Eukaryot. Cell 4:225229.
27. Hawker, L. E. 1965. Fine structure of fungi as revealed by electron microscopy. Biol. Rev. Camb. Phil. Soc. 40:5292.
28. Heath, I. B. 1986. Nuclear division: a marker for protist phylogeny? Prog. Protistol. 1:115162.
29. Hibbett, D. M.,, M. Binder,, J. F. Bischoff,, M. Blackwell,, P. F. Cannon,, O. Eriksson,, S. Huhndorf,, T. Y. James,, P. M. Kirk,, R. Lücking,, T. Lumbsch,, F. Lutzoni,, P. B. Matheny,, D. J. McLaughlin,, M. J. Powell,, S. Redhead,, C. L. Schoch,, J. W. Spatafora,, J. A. Stalpers,, R. Vilgalys,, M. C. Aime,, A. Aptroot,, R. Bauer,, D. Begerow,, G. L. Benny,, L. A. Castlebury,, P. W. Crous,, Y.-C. Dai,, W. Gams,, D. M. Geiser,, G. W. Griffith,, D. L. Hawksworth,, V. Hofstetter,, K. Hosaka,, R. A. Humber,, K. Hyde,, U. Kõljalg,, C. P. Kurtzman,, K.-H. Larsson,, R. Lichtwardt,, J. Longcore,, A. Miller,, J.-M. Moncalvo,, S. Mozley Standridge,, F. Oberwinkler,, E. Parmasto,, J. D. Rogers,, L. Ryvarden,, J. P. Sampaio,, A. Schuessler,, J. Sugiyama,, J. W. Taylor,, R. G. Thorn,, L. Tibell,, W. A. Untereiner,, C. Walker,, Z. Wang,, A. Weir,, M. Weiss,, M. White,, K. Winka,, Y.-J. Yao, and, N. Zhang. 2007. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111(Pt. 5):509547.
30. Hoch, H. C., and, R. C. Staples. 1985. The microtubule cytoskeleton in hyphae of Uromyces phaseoli germlings: its relationship to the region of nucleation and to the F-actin cytoskeleton. Protoplasma 124:112122.
31. Hohmann-Marriott, M. F.,, M. Uchida,, A. V. L. van de Meene,, M. Garret,, B. E. Hjelm,, S. Kokoori, and, R. W. Roberson. 2006. Electron tomography and its application to revealing fungal ultrastructure: Tansley Review. New Phytol. 172:208220.
32. Howard, R., and, J. R. Aist. 1979. Hyphal tip cell ultrastructure of the fungus Fusarium: improved preservation by freeze-substitution. J. Ultrastruct. Res. 66:224234.
33. Howard, R. J. 1981. Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze substitution. J. Cell Sci. 48:89103.
34. Hubbard, M. A., and, S. G. W. Kaminskyj. 2008. Rapid tip-directed movement of Golgi equivalents in growing Aspergillus nidulans hyphae suggests a mechanism for delivery of growth-related materials. Microbiology 154:15441553.
35. Jedd, G., and, N.-H. Chua. 2000. A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat. Cell Biol. 2:226231.
36. Kahn, S. R., and, J. W. Kimbrough. 1982. A reevaluation of the Basidiomycetes based upon septal and basidial structure. Mycotaxon 15:103120.
37. Knechtle, P.,, F. Dietrich, and, P. Philippsen. 2003. Maximal polar growth potential depends on the polarisoma component AgSpa2 in filamentous fungus Ashbya gossypii. Mol. Biol. Cell 14:41404154.
38. Kumar, T. K. A.,, G. J. Celio,, P. B. Brandon,, P. B. Matheny,, D. J. McLaughlin,, D. Hibbett, and, P. Manimohan. 2007. Phylogenetic relationships of Auriculoscypha based on ultrastructural and molecular studies. Mycol. Res. 111:268274.
39. López-Franco, R.,, S. Bartnicki-García, and, C. E. Bracker. 1994. Pulsed growth of fungal hyphal tips. Proc. Natl. Acad. Sci. USA 91:1222812232.
40. López-Franco, R.,, R. J. Howard, and, C. W. Bracker. 1995. Satellite Spitzenkörper in growing hyphal tips. Protoplasma 188:85103.
41. López-Franco, R., and, C. E. Bracker. 1996. Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195:90111.
42. Lutzoni, F.,, F. Kauff,, C. J. Caox,, D. McLaughlin,, G. Celio,, B. Dentinger,, M. Padamsee,, D. Hibbett,, T. Y. James,, E. Baloch,, M. Grube,, V. Reeb,, V. Hofstetter,, C. Schoch,, A. E. Arnold,, J. Miadlikowska,, J. Spatafora,, D. Johnson,, S. Hambleton,, M. Crockett,, R. Shoemaker,, G.-H. Sung,, R. Lücking,, T. Lumbsch,, K. O’Donnell,, M. Binder,, P. Diederich,, D. Ertz,, C. Gueidan,, K. Hansen,, R. C. Harris,, K. Hosaka,, Y.-W. Lim,, B. Matheny,, H. Nishida,, D. Pfister,, J. Rogers,, A. Rossman,, I. Schmitt,, H. Sipman,, J. Stone,, J. Sugiyama,, R. Yahr, and, R Vilgalys. 2004. Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am. J. Bot. 91:14461480.
43. Maruyama, J., and, K. Kitamoto. 2007. Differential distribution of the endoplasmic reticulum network in filamentous fungi. FEMS 272:17.
44. McDaniel, D. P., and, R. W. Roberson. 1998. γ-Tubulin is a component of the Spitzenkörper and centrosomes in hyphal tip cells of Allomyces macrogynus. Protoplasma 203:118123.
45. McDaniel, D. P., and, R. W. Roberson. 2000. Intracellular motility and mechanisms of control during hyphal tip growth in Allomyces. Fungal Genet. Biol. 31:223234.
46. McKerracher, L. J., and, I. B. Heath. 1985. The structure and cycle of the nucleus-associated organelle in two species of Basidiobolus. Mycologia 77:412417.
47. McLaughlin, D. J.,, M. E. Berres, and, L. J. Szabo. 1995. Molecules and morphology in basidiomycete phylogeny. Can. J. Bot. 73S:684692.
48. Momany, M.,, E. A. Richardson, and, G. Jedd. 2002. Mapping Woronin body position in Aspergillus nidulans. Mycologia 94:260266.
49. Morré, D. J.,, H. H. Mollenhauer, and, C. E. Bracker. 1971. Origin and continuity of Golgi apparatus, p. 82–126. In J. Reinert and, H. Ursprung (ed.), Results and Problems in Cell Differentiation. 2. Origin and Continuity of Cell Organelles. Springer, New York, NY.
50. Mouriño-Pérez, R. R.,, R. W. Roberson, and, S. BartnickiGarcía. 2006. Microtubule dynamics and organization during hyphal branching in Neurospora crassa. Fungal Genet. Biol. 43:389400.
51. Müller, W. H.,, A. J. Koster,, B. M. Humbel,, U. Ziese,, A. J. Verkleij,, A. C. Aelst,, T. P. van der Krift,, R. C. Montijn, and, T. Boekhout. 2000. Automated electron tomography of the septal pore cap in Rhizoctonia solani. J. Struct. Biol. 131:1018.
52. Oakley, C. E., and, B. R. Oakley. 1989. Identification of g-tubulin, a new member of the tubulin superfamily encoded by mip A gene of Aspergillus nidulans. Nature 338:662663.
53. Peñalva, M. A. 2005. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet. Biol. 42:963975.
54. Piper, R. C., and, D. J. Katzmann. 2007. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23:519547.
55. Pullan, W., and, H. Bhadeshia. 2000. Structure in Science and Art. Cambridge University Press, Cambridge, United Kingdom.
56. Read, N. D., and, E. R. Kalkman. 2003. Does endocytosis occur in fungal hyphae? Fungal Genet. Biol. 39:199203.
57. Riquelme, M., and, S. Bartnicki-García. 2004. Key differences between lateral and apical branching in hyphae of Neurospora crassa. Fungal Genet. Biol. 41:842851.
58. Riquelme, M.,, D. McDaniel,, R. W. Roberson, and, S. Bartnicki-García. 2002. The effect of ropy-1 mutation on cytoplasmic organization in mature hyphae of Neurospora crassa. Fungal Genet. Biol. 37:171179.
59. Riquelme, M.,, C. G. Reynaga-Peña,, G. Gierz, and, S. Bartnicki-García. 1998. What determines growth direction in fungal hyphae? Fungal Genet. Biol. 24:101109.
60. Riquelme, M.,, S. Bartnicki-García,, J. M. Gonzalez-Prieto,, E. Sánchez-Leon,, J. A. Verdín-Ramos,, A. BeltránAguilar, and, M. Freitag. 2007. Spitzenkörper localization and intracellular traffic of GFP-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot. Cell 6:18531864.
61. Roberson, R. W. 1992. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84:4151.
62. Roberson, R. W., and, M. S. Fuller. 1988. Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma 146:143149.
63. Roberson, R. W., and, M. S. Fuller. 1990. Effects of the sterol biosynthesis inhibitor cyproconazole on hyphal tip cells of Sclerotium rolfsii. II. An electron microscopic study. Exp. Mycol. 14:124135.
64. Roberson, R. W., and, M. M. Vargas. 1994. The tubulin cytoskeleton and its sites of nucleation in Allomyces macrogynus. Protoplasma 182:1931.
65. Sewall, T. C.,, R. W. Roberson, and, J. C. Pommerville. 1989. Identification and characterization of Golgi equivalents from Allomyces macrogynus. Exp. Mycol. 13:239252.
66. Sharpless, K. E., and, S. D. Harris. 2002. Functional characterization and localization of the Aspergillus nidulans formin SEPA. Mol. Biol. Cell 13:469479.
67. Soundararajan, S.,, G. Jedd,, X. Li,, M. Ramos-Pamplo ň;a, and, N. H. Chua. 2004. Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16:15641574.
68. Spellig, T.,, A. Bottin, and, R. Kahmann. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252:503509.
69. Srinivasan, S.,, M. M. Vargas, and, R. W. Roberson. 1996. Functional, organizational, and biochemical analysis of actin in the hyphal tip cells of Allomyces macrogynus. Mycologia 88:5780.
70. Suelmann, R., and, R. Fischer. 2000. Mitochondrial movement and morphology are dependent on an intact actin cytoskeleton in Aspergillus nidulans. Cell Motil. Cytoskelet. 45:4250.
71. Suelmann, R.,, N. Sievers, and, R. Fischer. 1997. Nuclear traffic in fungal hyphae: in vivo study of nuclear migration and position in Aspergillus nidulans. Mol. Microbiol. 45:4250.
72. Swann, E. C.,, E. M. Frieders, and, D. J. McLaughlin. 1999. Microbotryum, Kriegeria and the changing paradigm in basidiomycete classification. Mycologia 91:5166.
73. Taheri-Talesh, N.,, T. Horio,, L. Araujo-Bazán,, X. Dou,, E. A. Espeso,, M. A. Peñalva,, S. A. Osmani, and, B. R. Oakley. 2008. The tip growth apparatus of Aspergillus nidulans. Mol. Biol. Cell 19:14391449.
74. Trinci, A. P. J., and, A. J. Collinge. 1974. Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals. Protoplasma 80:5767.
75. Uchida, M.,, R. R. Mouriño-Pérez,, M. Freitag,, S. BartnickiGarcía, and, R. W. Roberson. 2008. Microtubule dynamics and the role of molecular motors in Neurospora crassa. Fungal Genet. Biol. 45:683692.
76. Upadhyay, S., and, B. D. Shaw. 2008. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol. Microbiol. 178:131141.
77. van Driel, K. G. A.,, A. F. van Peer,, J. Grijpstra,, H. A. B. Wösten,, A. J. Verkleij,, W. H. Muller, and, T. Boekhout. 2008. Septal pore cap protein SPC18, isolated from the basidiomycetous fungus Rhizoctonia solani, also resides in pore plugs. Eukaryot. Cell 7:18651873.
78. Vargas, M. M.,, J. M. Aronson, and, R. W. Roberson. 1993. The cytoplasmic organization of hyphal tip cells in the fungus Allomyces macrogynus. Protoplasma 176:4352.
79. Veses, V.,, A. Richards, and, N. A. R. Gow. 2008. Vacuoles and fungal biology. Curr. Opin. Microbiol. 11:503510.
80. Virag, A., and, A. J. F. Griffiths. 2004. A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet. Biol. 41:213225.
81. White, M. M.,, T. Y. James,, K. O’Donnell,, M. J. Cafaro,, Y. Tanabe, and, J. Sugiyama. 2006. Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98:872884.
82. Zekert, N., and, R. Fischer. 2009. The Aspergillus nidulans kinesin-3 UncA motor moves vesicles along a subpopulation of microtubules. Mol. Biol. Cell 20:673684.

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