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Chapter 11 : Cell Biology of Hyphal Growth

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Abstract:

Filamentous fungi are a large and ancient clade of microorganisms that occupy a broad range of ecological niches ( ). Fungi are recyclers, being major decomposers of plant debris ( ); they form mycorrhizal symbiosis with 93% of all flowering plant families ( ), and they serve in the industrial production of proteins ( ). However, fungi pose a threat to public health, the ecosystem, and our food security ( ). The success of filamentous fungi is largely due to their elongate hypha, a chain of cells separated from each other by septa ( ). Hyphae grow rapidly by polarized exocytosis at the apex ( ), which allows the fungus to extend over long distances and invade many substrates, including soils and host tissues. Hyphal tip growth is initiated by establishment of a growth site and the subsequent maintenance of the growth axis, with transport of growth supplies, including membranes and proteins, delivered by motors along the cytoskeleton to the hyphal apex ( ). Among the enzymes delivered are cell wall synthases that are exocytosed for local synthesis of the extracellular cell wall ( ). Exocytosis is opposed by endocytic uptake of soluble and membrane-bound material into the cell ( ). The first intracellular compartment in the endocytic pathway is the early endosomes (EEs), which emerge to perform essential additional functions as spatial organizers of the hyphal cell ( ). Individual compartments within septated hyphae can communicate with each other via septal pores, which allow passage of cytoplasm or organelles ( ) to help differentiation within the mycelium ( ). This article introduces the reader to more detailed aspects of hyphal growth in fungi.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 1
Figure 1

Growth patterns in fungal hyphae. Growth occurs in an isotropic fashion during spore germination. Specification of a polarity axis ultimately results in the formation of a hypha that continues to grow at the tip. While tip growth is maintained, the specification of additional polarity axes enables the formation of septa and lateral branches. Whereas septum formation is transient, branching results in the formation of a secondary hypha that also continues to grow at the tip. Red arrows designate polarity axes.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 2
Figure 2

Highly schematic representation of the cisternal maturation process in the nonstacked fungal Golgi, with indication of the different functional stages. COPII-coated vesicles (green) bud off specialized domains of the ER denoted ER exit sites (ERES) or transitional ER (left). COPII vesicles coalesce to form an early Golgi cisterna, represented here as a green fenestrated structure that depicts actual Golgi structures often visible in EM micrographs. Retrograde COPI traffic (violet vesicles) retrieves back to the ER proteins such as cargo receptors that need to be recycled. Early cisternae are equipped with cargo glycosylation enzymes (t0). As time passes (double arrowheads) an early Golgi cisterna becomes progressively enriched in cargo and late Golgi components (represented in red) by delivering early Golgi ones (e.g., glycosylating enzymes) to cisternae in earlier stages of maturation, in a process which is likely mediated by COPI retrograde traffic (t1 and t2). Eventually, late Golgi components become predominate (TGN, t3) and the cargo-enriched cisterna becomes competent to tear off into carriers destined for the plasma membrane (PM) and the endosomes (t4). TGN cisternae also receive traffic from the endosomal system (blue arrows). In the route (dark blue) connecting the cisternae with the PM, the transition between late Golgi and post-Golgi identity is dictated by the recruitment of RabE to the membranes, which is critically regulated by TRAPPII (see text). Proteins that have been shown by microscopy to localize to specific stages are indicated, with green lettering indicating early Golgi and red lettering indicating TGN. The image summarizes work performed with .

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 3

Illustration of a hyphal tip with the main organelles and subcellular components involved in apical cell wall growth. The diagram is based on work with . (Art: Leonora Martínez-Núñez).

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 4

Diagram showing the cooperation of molecular motors in bidirectional EE motility. The illustration is based on results obtained from studies of . See text for detailed description.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 5
Figure 5

EEs as multifunctional platforms. Proteins that associate with the organelles are shown as colored symbols and described in black; functions are indicated in dark red. The diagram is based on work with , , and . See text for detailed description.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 6
Figure 6

Time course of the contraction of the CAR during septum formation in the wheat pathogen . The side view of the three-dimensional image stack shows that the CAR is closing with time. Time in minutes is shown in the upper-left corners. The CAR was labeled using an F-actin-specific GFP-LifeAct probe.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 7
Figure 7

Model for septum formation. A signal emanating from mitotic nuclei is relayed to the septation site via the septation initiation network (SIN). Components needed for assembly of the contractile actin ring (CAR) (actin filaments, Bud4) are already associated with the septation site and operate in conjunction with the SIN to define the division plane. Activation of the GTPase Rho4 at the septation site initiates organization of actin filaments into a CAR. Constriction of the CAR is coincident with appearance of a septin ring. Deposition of the septum is guided by the CAR. The septin ring disassembles once the final size of the septal pore is reached. Several proteins, including calcineurin and Rho4, remain associated with the mature septal pore. The diagram was modified from Beck et al. ( ).

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 8
Figure 8

Model for tip-ward translocation in . Newly formed hyphal compartments are in cytoplasmic contact with neighboring cells. The Woronin body is not plugging the septal pore, and cytoplasmic streaming, as well as diffusion through the septal pore, is possible (green arrow). Older septa are plugged by Woronin bodies, which prevents exchange of cytoplasm. However, selective transport of molecules such as glucose toward the growth region is still possible (red arrows). This may involve septum-associated transporters.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 9
Figure 9

Schematic drawing of a dolipore in the basidiomycete . The image was redrawn from a reconstruction of electron micrographs, first published in reference .

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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References

/content/book/10.1128/9781555819583.chap11
1. Berbee ML,, Taylor JW . 2010. Dating the molecular clock in fungi: how close are we? Fungal Biol Rev 24 : 116.[CrossRef] [PubMed]
2. Stajich JE,, Berbee ML,, Blackwell M,, Hibbett DS,, James TY,, Spatafora JW,, Taylor JW . 2009. The fungi. Curr Biol 19 : R840R845.[CrossRef]
3. Evans CS,, Hedger JN, . 2001. Degradation of plant cell wall polymers, p 126. In Gadd GM (ed), Fungi in Bioremediation. Cambridge University Press, Cambridge, United Kingdom.[CrossRef]
4. Brundrett MC . 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320 : 3777.[CrossRef]
5. Iwashita K . 2002. Recent studies of protein secretion by filamentous fungi. J Biosci Bioeng 94 : 530535.[CrossRef]
6. Brown GD,, Denning DW,, Gow NA,, Levitz SM,, Netea MG,, White TC . 2012. Hidden killers: human fungal infections. Sci Transl Med 4 : 165rv13.[CrossRef] [PubMed]
7. Fisher MC,, Henk DA,, Briggs CJ,, Brownstein JS,, Madoff LC,, McCraw SL,, Gurr SJ . 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484 : 186194.[CrossRef] [PubMed]
8. Harris SD . 2001. Septum formation in Aspergillus nidulans . Curr Opin Microbiol 4 : 736739.[CrossRef]
9. Bartnicki-Garcia S,, Lippman E . 1969. Fungal morphogenesis: cell wall construction in Mucor rouxii . Science 165 : 302304.[CrossRef] [PubMed]
10. Reinhardt MO . 1892. Das Wachstum von Pilzhyphen. Jahrb Wiss Bot 23 : 479566.
11. Wessels JGH . 1988. A steady-state model for apical wall growth in fungi. Acta Bot Neerl 37 : 316.[CrossRef]
12. Steinberg G . 2007. Hyphal growth: a tale of motors, lipids, and the Spitzenkörper. Eukaryot Cell 6 : 351360.[PubMed] [CrossRef]
13. Riquelme M,, Roberson RW,, Sánchez-León E, . 2016. Hyphal tip growth in filamentous fungi, p 4766. In Wendland J (ed), Growth, Differentiation and Sexuality, vol. I, 3rd ed. Springer International Publishing, Cham, Switzerland.
14. Peñalva MA . 2010. Endocytosis in filamentous fungi: Cinderella gets her reward. Curr Opin Microbiol 13 : 684692.[CrossRef] [PubMed]
15. Steinberg G . 2014. Endocytosis and early endosome motility in filamentous fungi. Curr Opin Microbiol 20 : 1018.[CrossRef] [PubMed]
16. Jedd G,, Pieuchot L . 2012. Multiple modes for gatekeeping at fungal cell-to-cell channels. Mol Microbiol 86 : 12911294.[CrossRef] [PubMed]
17. Wösten HA,, van Veluw GJ,, de Bekker C,, Krijgsheld P . 2013. Heterogeneity in the mycelium: implications for the use of fungi as cell factories. Biotechnol Lett 35 : 11551164.[PubMed] [CrossRef]
18. Harris SD . 2011. Hyphal morphogenesis: an evolutionary perspective. Fungal Biol 115 : 475484.[CrossRef] [PubMed]
19. Celio GJ,, Padamsee M,, Dentinger BT,, Bauer R,, McLaughlin DJ . 2006. Assembling the fungal tree of life: constructing the structural and biochemical database. Mycologia 98 : 850859.[CrossRef] [PubMed]
20. Harris SD, . 2010. Hyphal growth and polarity, p 238259. In Borkovich KA,, Ebbole DJ (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC.
21. Riquelme M . 2013. Tip growth in filamentous fungi: a road trip to the apex. Annu Rev Microbiol 67 : 587609.[CrossRef] [PubMed]
22. Chang F,, Peter M . 2003. Yeasts make their mark. Nat Cell Biol 5 : 294299.[CrossRef] [PubMed]
23. Turrà D,, El Ghalid M,, Rossi F,, Di Pietro A . 2015. Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527 : 521524.[CrossRef]
24. Chant J . 1999. Cell polarity in yeast. Annu Rev Cell Dev Biol 15 : 365391.[CrossRef]
25. Chang F,, Martin SG . 2009. Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol 1 : a001347.[CrossRef] [PubMed]
26. Fischer R,, Zekert N,, Takeshita N . 2008. Polarized growth in fungi: interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68 : 813826.[CrossRef]
27. 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 : 220235.[CrossRef]
28. Si H,, Justa-Schuch D,, Seiler S,, Harris SD . 2010. Regulation of septum formation by the Bud3-Rho4 GTPase module in Aspergillus nidulans . Genetics 185 : 165176.[CrossRef]
29. Harris SD . 1999. Morphogenesis is coordinated with nuclear division in germinating Aspergillus nidulans conidiospores. Microbiology 145 : 27472756.[CrossRef]
30. Konzack S,, Rischitor PE,, Enke C,, Fischer R . 2005. The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans . Mol Biol Cell 16 : 497506.[CrossRef] [PubMed]
31. Harris SD . 2008. Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems. Mycologia 100 : 823832.[CrossRef] [PubMed]
32. Si H,, Rittenour WR,, Harris SD . 2016. Roles of Aspergillus nidulans Cdc42/Rho GTPase regulators in hyphal morphogenesis and development. Mycologia 108 : 543555.[CrossRef]
33. DeMay BS,, Meseroll RA,, Occhipinti P,, Gladfelter AS . 2009. Regulation of distinct septin rings in a single cell by Elm1p and Gin4p kinases. Mol Biol Cell 20 : 23112326.[CrossRef] [PubMed]
34. Bridges AA,, Jentzsch MS,, Oakes PW,, Occhipinti P,, Gladfelter AS . 2016. Micron-scale plasma membrane curvature is recognized by the septin cytoskeleton. J Cell Biol 213 : 2332.[CrossRef]
35. Semighini CP,, Harris SD . 2008. Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 179 : 19191932.[CrossRef]
36. Takemoto D,, Tanaka A,, Scott B . 2006. A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18 : 28072821.[CrossRef]
37. Taheri-Talesh N,, Horio T,, Araujo-Bazán L,, Dou X,, Espeso EA,, Peñalva MA,, Osmani SA,, Oakley BR . 2008. The tip growth apparatus of Aspergillus nidulans . Mol Biol Cell 19 : 14391449.[CrossRef] [PubMed]
38. Upadhyay S,, Shaw BD . 2008. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans . Mol Microbiol 68 : 690705.[CrossRef] [PubMed]
39. Schultzhaus Z,, Yan H,, Shaw BD . 2015. Aspergillus nidulans flippase DnfA is cargo of the endocytic collar and plays complementary roles in growth and phosphatidylserine asymmetry with another flippase, DnfB. Mol Microbiol 97 : 1832.[CrossRef]
40. Shaw BD,, Chung DW,, Wang CL,, Quintanilla LA,, Upadhyay S . 2011. A role for endocytic recycling in hyphal growth. Fungal Biol 115 : 541546.[CrossRef] [PubMed]
41. Takeshita N,, Higashitsuji Y,, Konzack S,, Fischer R . 2008. Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans . Mol Biol Cell 19 : 339351.[CrossRef]
42. Ishitsuka Y,, Savage N,, Li Y,, Bergs A,, Grün N,, Kohler D,, Donnelly R,, Nienhaus GU,, Fischer R,, Takeshita N . 2015. Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth. Sci Adv 1 : e1500947.[CrossRef]
43. Pearson CL,, Xu K,, Sharpless KE,, Harris SD . 2004. MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans . Mol Biol Cell 15 : 36583672.[PubMed] [CrossRef]
44. Takeshita N,, Diallinas G,, Fischer R . 2012. The role of flotillin FloA and stomatin StoA in the maintenance of apical sterol-rich membrane domains and polarity in the filamentous fungus Aspergillus nidulans . Mol Microbiol 83 : 11361152.[CrossRef]
45. Chang F,, Minc N . 2014. Electrochemical control of cell and tissue polarity. Annu Rev Cell Dev Biol 30 : 317336.[CrossRef] [PubMed]
46. Thomson DD,, Wehmeier S,, Byfield FJ,, Janmey PA,, Caballero-Lima D,, Crossley A,, Brand AC . 2015. Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae. Cell Microbiol 17 : 342354.[CrossRef]
47. Lew DJ,, Reed SI . 1995. Cell cycle control of morphogenesis in budding yeast. Curr Opin Genet Dev 5 : 1723.[CrossRef]
48. Wang Y . 2009. CDKs and the yeast-hyphal decision. Curr Opin Microbiol 12 : 644649.[CrossRef] [PubMed]
49. Li CR,, Au Yong JY,, Wang YM,, Wang Y . 2012. CDK regulates septin organization through cell-cycle-dependent phosphorylation of the Nim1-related kinase Gin4. J Cell Sci 125 : 25332543.[CrossRef]
50. Wang H,, Huang ZX,, Au Yong JY,, Zou H,, Zeng G,, Gao J,, Wang Y,, Wong AH,, Wang Y . 2016. CDK phosphorylates the polarisome scaffold Spa2 to maintain its localization at the site of cell growth. Mol Microbiol 101 : 250264.[CrossRef] [PubMed]
51. Sgarlata C,, Pérez-Martín J . 2005. Inhibitory phosphorylation of a mitotic cyclin-dependent kinase regulates the morphogenesis, cell size and virulence of the smut fungus Ustilago maydis . J Cell Sci 118 : 36073622.[CrossRef]
52. Morris NR . 1975. Mitotic mutants of Aspergillus nidulans . Genet Res 26 : 237254.[CrossRef]
53. Fiddy C,, Trinci AP . 1976. Mitosis, septation, branching and the duplication cycle in Aspergillus nidulans . J Gen Microbiol 97 : 169184.[CrossRef] [PubMed]
54. Momany M,, Taylor I . 2000. Landmarks in the early duplication cycles of Aspergillus fumigatus and Aspergillus nidulans: polarity, germ tube emergence and septation. Microbiology 146 : 32793284.[CrossRef] [PubMed]
55. Gladfelter AS,, Hungerbuehler AK,, Philippsen P . 2006. Asynchronous nuclear division cycles in multinucleated cells. J Cell Biol 172 : 347362.[CrossRef] [PubMed]
56. Bergen LG,, Upshall A,, Morris NR . 1984. S-phase, G2, and nuclear division mutants of Aspergillus nidulans . J Bacteriol 159 : 114119.[PubMed]
57. Peñalva MA,, Galindo A,, Abenza JF,, Pinar M,, Calcagno-Pizarelli AM,, Arst HN,, Pantazopoulou A . 2012. Searching for gold beyond mitosis: mining intracellular membrane traffic in Aspergillus nidulans . Cell Logist 2 : 214.[CrossRef]
58. Harris SD,, Hofmann AF,, Tedford HW,, Lee MP . 1999. Identification and characterization of genes required for hyphal morphogenesis in the filamentous fungus Aspergillus nidulans . Genetics 151 : 10151025.[PubMed]
59. Momany M,, Westfall PJ,, Abramowsky G . 1999. Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics 151 : 557567.[PubMed]
60. Pinar M,, Pantazopoulou A,, Arst HN Jr,, Peñalva MA . 2013. Acute inactivation of the Aspergillus nidulans Golgi membrane fusion machinery: correlation of apical extension arrest and tip swelling with cisternal disorganization. Mol Microbiol 89 : 228248.[CrossRef]
61. Malhotra V . 2013. Unconventional protein secretion: an evolving mechanism. EMBO J 32 : 16601664.[PubMed] [CrossRef]
62. Klumperman J . 2011. Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3 : a005181.[CrossRef] [PubMed]
63. Pantazopoulou A . 2016. The Golgi apparatus: insights from filamentous fungi. Mycologia 108 : 603622.[CrossRef] [PubMed]
64. Pantazopoulou A,, Peñalva MA . 2011. Characterization of Aspergillus nidulans RabC/Rab6. Traffic 12 : 386406.[CrossRef] [PubMed]
65. Sánchez-León E,, Bowman B,, Seidel C,, Fischer R,, Novick P,, Riquelme M . 2015. The Rab GTPase YPT-1 associates with Golgi cisternae and Spitzenkörper microvesicles in Neurospora crassa . Mol Microbiol 95 : 472490.[CrossRef]
66. Wooding S,, Pelham HRB . 1998. The dynamics of Golgi protein traffic visualized in living yeast cells. Mol Biol Cell 9 : 26672680.[CrossRef] [PubMed]
67. Breakspear A,, Langford KJ,, Momany M,, Assinder SJ . 2007. CopA:GFP localizes to putative Golgi equivalents in Aspergillus nidulans . FEMS Microbiol Lett 277 : 9097.[CrossRef] [PubMed]
68. Pantazopoulou A,, Peñalva MA . 2009. Organization and dynamics of the Aspergillus nidulans Golgi during apical extension and mitosis. Mol Biol Cell 20 : 43354347.[CrossRef] [PubMed]
69. Glick BS,, Luini A . 2011. Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3 : a005215.[CrossRef]
70. Losev E,, Reinke CA,, Jellen J,, Strongin DE,, Bevis BJ,, Glick BS . 2006. Golgi maturation visualized in living yeast. Nature 441 : 10021006.[CrossRef] [PubMed]
71. Matsuura-Tokita K,, Takeuchi M,, Ichihara A,, Mikuriya K,, Nakano A . 2006. Live imaging of yeast Golgi cisternal maturation. Nature 441 : 10071010.[CrossRef] [PubMed]
72. Patterson GH,, Hirschberg K,, Polishchuk RS,, Gerlich D,, Phair RD,, Lippincott-Schwartz J . 2008. Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133 : 10551067.[CrossRef]
73. Papanikou E,, Glick BS . 2014. Golgi compartmentation and identity. Curr Opin Cell Biol 29 : 7481.[CrossRef] [PubMed]
74. Bonifacino JS,, Glick BS . 2004. The mechanisms of vesicle budding and fusion. Cell 116 : 153166.[CrossRef]
75. López-Berges MS,, Pinar M,, Abenza JF,, Arst HN Jr,, Peñalva MA . 2016. The Aspergillus nidulans syntaxin PepA(Pep12) is regulated by two Sec1/Munc-18 proteins to mediate fusion events at early endosomes, late endosomes and vacuoles. Mol Microbiol 99 : 199216.[CrossRef] [PubMed]
76. Stanley P . 2011. Golgi glycosylation. Cold Spring Harb Perspect Biol 3 : a005199.[CrossRef] [PubMed]
77. Jackson-Hayes L,, Hill TW,, Loprete DM,, Fay LM,, Gordon BS,, Nkashama SA,, Patel RK,, Sartain CV . 2008. Two GDP-mannose transporters contribute to hyphal form and cell wall integrity in Aspergillus nidulans . Microbiology 154 : 20372047.[CrossRef]
78. Whyte JR,, Munro S . 2001. The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev Cell 1 : 527537.[CrossRef]
79. Ungar D,, Oka T,, Krieger M,, Hughson FM . 2006. Retrograde transport on the COG railway. Trends Cell Biol 16 : 113120.[CrossRef] [PubMed]
80. Gremillion SK,, Harris SD,, Jackson-Hayes L,, Kaminskyj SG,, Loprete DM,, Gauthier AC,, Mercer S,, Ravita AJ,, Hill TW . 2014. Mutations in proteins of the conserved oligomeric golgi complex affect polarity, cell wall structure, and glycosylation in the filamentous fungus Aspergillus nidulans . Fungal Genet Biol 73 : 6982.[CrossRef]
81. Arst HN Jr,, Hernández-González M,, Peñalva MA,, Pantazopoulou A . 2014. GBF/Gea mutant with a single substitution sustains fungal growth in the absence of BIG/Sec7. FEBS Lett 588 : 47994806.[CrossRef] [PubMed]
82. Pantazopoulou A,, Pinar M,, Xiang X,, Peñalva MA . 2014. Maturation of late Golgi cisternae into RabERAB11 exocytic post-Golgi carriers visualized in vivo . Mol Biol Cell 25 : 24282443.[CrossRef]
83. Pinar M,, Arst HN Jr,, Pantazopoulou A,, Tagua VG,, de los Ríos V,, Rodríguez-Salarichs J,, Díaz JF,, Peñalva MA . 2015. TRAPPII regulates exocytic Golgi exit by mediating nucleotide exchange on the Ypt31 ortholog RabERAB11. Proc Natl Acad Sci USA 112 : 43464351.[CrossRef] [PubMed]
84. Pinar M,, Pantazopoulou A,, Peñalva MA . 2013. Live-cell imaging of Aspergillus nidulans autophagy: RAB1 dependence, Golgi independence and ER involvement. Autophagy 9 : 10241043.[CrossRef]
85. Levine TP,, Munro S . 2002. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol 12 : 695704.[CrossRef]
86. Daboussi L,, Costaguta G,, Payne GS . 2012. Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat Cell Biol 14 : 239248.[CrossRef] [PubMed]
87. Schultzhaus Z,, Johnson TB,, Shaw BD . 2017. Clathrin localization and dynamics in Aspergillus nidulans . Mol Microbiol 103 : 299318.[CrossRef]
88. Abenza JF,, Pantazopoulou A,, Rodríguez JM,, Galindo A,, Peñalva MA . 2009. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10 : 5775.[CrossRef]
89. 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 : 246259.[CrossRef]
90. Valdez-Taubas J,, Pelham HR . 2003. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr Biol 13 : 16361640.[CrossRef]
91. Gilbert MJ,, Thornton CR,, Wakley GE,, Talbot NJ . 2006. A P-type ATPase required for rice blast disease and induction of host resistance. Nature 440 : 535539.[CrossRef]
92. Hernández-González M,, Peñalva MA,, Pantazopoulou A . 2015. Conditional inactivation of Aspergillus nidulans sarA(SAR1) uncovers the morphogenetic potential of regulating endoplasmic reticulum (ER) exit. Mol Microbiol 95 : 491508.[CrossRef]
93. Veldhuisen G,, Saloheimo M,, Fiers MA,, Punt PJ,, Contreras R,, Penttilä M,, van den Hondel CA . 1997. Isolation and analysis of functional homologues of the secretion-related SAR1 gene of Saccharomyces cerevisiae from Aspergillus niger and Trichoderma reesei . Mol Gen Genet 256 : 446455.
94. Lee SC,, Shaw BD . 2008. Localization and function of ADP ribosylation factor A in Aspergillus nidulans . FEMS Microbiol Lett 283 : 216222.[CrossRef] [PubMed]
95. Morozova N,, Liang Y,, Tokarev AA,, Chen SH,, Cox R,, Andrejic J,, Lipatova Z,, Sciorra VA,, Emr SD,, Segev N . 2006. TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nat Cell Biol 8 : 12631269.[CrossRef]
96. Cai Y,, Chin HF,, Lazarova D,, Menon S,, Fu C,, Cai H,, Sclafani A,, Rodgers DW,, De La Cruz EM,, Ferro-Novick S,, Reinisch KM . 2008. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133 : 12021213.[CrossRef]
97. Yang Y,, El-Ganiny AM,, Bray GE,, Sanders DAR,, Kaminskyj SGW . 2008. Aspergillus nidulans hypB encodes a Sec7-domain protein important for hyphal morphogenesis. Fungal Genet Biol 45 : 749759.[CrossRef] [PubMed]
98. Girbardt M . 1957. Der Spitzenkörper von Polystictus versicolor . Planta 50 : 4759.[CrossRef]
99. Girbardt M . 1969. Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma 67 : 413441.[CrossRef]
100. López-Franco R,, Bracker CE . 1996. Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195 : 90111.[CrossRef]
101. Chapa-y-Lazo B,, Lee S,, Regan H,, Sudbery P . 2011. The mating projections of Saccharomyces cerevisiae and Candida albicans show key characteristics of hyphal growth. Fungal Biol 115 : 547556.[CrossRef] [PubMed]
102. Hoch HC,, Staples RC . 1983. Ultrastructural organization of the nondifferentiated uredospore germling of Uromyces phaseoli variety typica. Mycologia 75 : 795824.[CrossRef]
103. Lehmler C,, Steinberg G,, Snetselaar KM,, Schliwa M,, Kahmann R,, Bölker M . 1997. Identification of a motor protein required for filamentous growth in Ustilago maydis . EMBO J 16 : 34643473.[CrossRef] [PubMed]
104. Roberson RW,, Saucedo E,, Maclean D,, Propster J,, Unger B,, Oneil TA,, Parvanehgohar K,, Cavanaugh C,, Lowry D . 2011. The hyphal tip structure of Basidiobolus sp.: a zygomycete fungus of uncertain phylogeny. Fungal Biol 115 : 485492.[CrossRef]
105. Vargas M,, Aronson JM,, Roberson RW . 1993. The cytoplasmic organization of hyphal tip cells in the fungus Allomyces macrogynus . Protoplasma 176 : 4352.[CrossRef]
106. McClure WK,, Park D,, Robinson PM . 1968. Apical organization in the somatic hyphae of fungi. J Gen Microbiol 50 : 177182.[CrossRef] [PubMed]
107. Fisher KE,, Roberson RW . 2016. Fungal hyphal growth: Spitzenkörper versus apical vesicle crescent. Fungal Genom Biol 6 : 136.
108. Fisher KE,, Roberson RW . 2016. Hyphal tip cytoplasmic organization in four zygomycetous fungi. Mycologia 108 : 533542.[CrossRef] [PubMed]
109. Bartnicki-Garcia S, . 1973. Fundamental aspects of hyphal morphogenesis, p 245267. In Ashworth JM,, Smith E (ed), Microbial Differentiation. Cambridge University Press, Cambridge, United Kingdom.
110. Green PB . 1969. Cell morphogenesis. Annu Rev Plant Pathol 20 : 365394.[CrossRef]
111. Robertson NF . 1965. Presidential address: the fungal hypha. Trans Br Mycol Soc 48 : 18.[CrossRef]
112. Martínez-Núñez L,, Riquelme M . 2015. Role of BGT-1 and BGT-2, two predicted GPI-anchored glycoside hydrolases/glycosyltransferases, in cell wall remodeling in Neurospora crassa . Fungal Genet Biol 85 : 5870.[CrossRef]
113. Bourett TM,, Howard RJ . 1991. Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163 : 199202.[CrossRef]
114. Grove SN,, Bracker CE . 1970. Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J Bacteriol 104 : 9891009.[PubMed]
115. Bartnicki-Garcia S,, Hergert F,, Gierz G . 1989. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal tip growth. Protoplasma 153 : 4657.[CrossRef]
116. Latgé JP,, Calderone R, . 2006. The fungal cell wall, p 73104. In Kues U,, Fischer R (ed), The Mycota, vol. 1, Springer-Verlag, Berlin, Germany.
117. Sietsma JH,, Wessels JGH, . 2006. Apical wall biogenesis, p 5372. In Kues U,, Fischer R (ed), The Mycota, Vol. 1. Springer-Verlag, Berlin, Germany.
118. Riquelme M,, Bartnicki-García S,, González-Prieto JM,, Sánchez-León E,, Verdín-Ramos JA,, Beltrán-Aguilar A,, Freitag M . 2007. Spitzenkorper 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 : 18531864.[CrossRef]
119. Verdín J,, Bartnicki-Garcia S,, Riquelme M . 2009. Functional stratification of the Spitzenkörper of Neurospora crassa . Mol Microbiol 74 : 10441053.[CrossRef]
120. Riquelme M,, Bredeweg EL,, Callejas-Negrete O,, Roberson RW,, Ludwig S,, Beltrán-Aguilar A,, Seiler S,, Novick P,, Freitag M . 2014. The Neurospora crassa exocyst complex tethers Spitzenkörper vesicles to the apical plasma membrane during polarized growth. Mol Biol Cell 25 : 13121326.[CrossRef]
121. Peñalva MA . 2015. A lipid-managing program maintains a stout Spitzenkörper. Mol Microbiol 97 : 16.[CrossRef]
122. Bartnicki-Garcia S, . 2002. Hyphal tip growth: outstanding questions, p 2958. In Osiewacz HD , Molecular Biology of Fungal Development. Marcel Dekker, New York, NY.
123. Harris SD,, Read ND,, Roberson RW,, Shaw B,, Seiler S,, Plamann M,, Momany M . 2005. Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryot Cell 4 : 225229.[CrossRef] [PubMed]
124. Berepiki A,, Lichius A,, Shoji JY,, Tilsner J,, Read ND . 2010. F-actin dynamics in Neurospora crassa . Eukaryot Cell 9 : 547557.[CrossRef] [PubMed]
125. Delgado-Álvarez DL,, Callejas-Negrete OA,, Gómez N,, Freitag M,, Roberson RW,, Smith LG,, Mouriño-Pérez RR . 2010. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa . Fungal Genet Biol 47 : 573586.[CrossRef]
126. Takeshita N,, Mania D,, Herrero S,, Ishitsuka Y,, Nienhaus GU,, Podolski M,, Howard J,, Fischer R . 2013. The cell-end marker TeaA and the microtubule polymerase AlpA contribute to microtubule guidance at the hyphal tip cortex of Aspergillus nidulans to provide polarity maintenance. J Cell Sci 126 : 54005411.[CrossRef]
127. Horio T,, Oakley BR . 2005. The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans . Mol Biol Cell 16 : 918926.[CrossRef] [PubMed]
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 : 17431752.[CrossRef]
129. Caballero-Lima D,, Kaneva IN,, Watton SP,, Sudbery PE,, Craven CJ . 2013. The spatial distribution of the exocyst and actin cortical patches is sufficient to organize hyphal tip growth. Eukaryot Cell 12 : 9981008.[CrossRef]
130. Riquelme M,, Reynaga-Peña CG,, Gierz G,, Bartnicki-García S . 1998. What determines growth direction in fungal hyphae? Fungal Genet Biol 24 : 101109.[CrossRef]
131. Vida TA,, Emr SD . 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128 : 779792.[CrossRef]
132. 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 : 24762494.[CrossRef]
133. James TY,, Pelin A,, Bonen L,, Ahrendt S,, Sain D,, Corradi N,, Stajich JE . 2013. Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. Curr Biol 23 : 15481553.[CrossRef] [PubMed]
134. 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 : 225242.[CrossRef]
135. Schuster M,, Treitschke S,, Kilaru S,, Molloy J,, Harmer NJ,, Steinberg G . 2012. Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J 31 : 214227.[CrossRef] [PubMed]
136. Schuster M,, Martin-Urdiroz M,, Higuchi Y,, Hacker C,, Kilaru S,, Gurr SJ,, Steinberg G . 2016. Co-delivery of cell-wall-forming enzymes in the same vesicle for coordinated fungal cell wall formation. Nat Microbiol 1 : 16149.[CrossRef]
137. Fujiwara M,, Horiuchi H,, Ohta A,, Takagi M . 1997. A novel fungal gene encoding chitin synthase with a myosin motor-like domain. Biochem Biophys Res Commun 236 : 7578.[CrossRef] [PubMed]
138. Aufauvre-Brown A,, Mellado E,, Gow NA,, Holden DW . 1997. Aspergillus fumigatus chsE: a gene related to CHS3 of Saccharomyces cerevisiae and important for hyphal growth and conidiophore development but not pathogenicity. Fungal Genet Biol 21 : 141152.[CrossRef] [PubMed]
139. Jiménez-Ortigosa C,, Aimanianda V,, Muszkieta L,, Mouyna I,, Alsteens D,, Pire S,, Beau R,, Krappmann S,, Beauvais A,, Dufrêne YF,, Roncero C,, Latgé JP . 2012. Chitin synthases with a myosin motor-like domain control the resistance of Aspergillus fumigatus to echinocandins. Antimicrob Agents Chemother 56 : 61216131.[CrossRef]
140. Madrid MP,, Di Pietro A,, Roncero MI . 2003. Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Mol Microbiol 47 : 257266.[CrossRef]
141. Werner S,, Sugui JA,, Steinberg G,, Deising HB . 2007. A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation, and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola . Mol Plant Microbe Interact 20 : 15551567.[CrossRef]
142. Kong LA,, Yang J,, Li GT,, Qi LL,, Zhang YJ,, Wang CF,, Zhao WS,, Xu JR,, Peng YL . 2012. Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporth eoryzae . PLoS Pathog 8 : e1002526.[CrossRef]
143. Fajardo-Somera RA,, Jöhnk B,, Bayram Ö,, Valerius O,, Braus GH,, Riquelme M . 2015. Dissecting the function of the different chitin synthases in vegetative growth and sexual development in Neurospora crassa . Fungal Genet Biol 75 : 3045.[CrossRef]
144. Horiuchi H,, Fujiwara M,, Yamashita S,, Ohta A,, Takagi M . 1999. Proliferation of intrahyphal hyphae caused by disruption of csmA, which encodes a class V chitin synthase with a myosin motor-like domain in Aspergillus nidulans . J Bacteriol 181 : 37213729.[PubMed]
145. Takeshita N,, Wernet V,, Tsuizaki M,, Grün N,, Hoshi HO,, Ohta A,, Fischer R,, Horiuchi H . 2015. Transportation of Aspergillus nidulans class III and V chitin synthases to the hyphal tips depends on conventional kinesin. PLoS One 10 : e0125937.[CrossRef]
146. 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 : 19611970.[CrossRef]
147. Read ND,, Kalkman ER . 2003. Does endocytosis occur in fungal hyphae? Fungal Genet Biol 39 : 199203.[CrossRef]
148. Hoffmann J,, Mendgen K . 1998. Endocytosis and membrane turnover in the germ tube of Uromyces fabae . Fungal Genet Biol 24 : 7785.[CrossRef] [PubMed]
149. Steinberg G,, Schliwa M,, Lehmler C,, Bölker M,, Kahmann R,, McIntosh JR . 1998. Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J Cell Sci 111 : 22352246.[PubMed]
150. Atkinson HA,, Daniels A,, Read ND . 2002. Live-cell imaging of endocytosis during conidial germination in the rice blast fungus, Magnaporthe grisea . Fungal Genet Biol 37 : 233244.[CrossRef]
151. Peñalva MA . 2005. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet Biol 42 : 963975.[CrossRef] [PubMed]
152. Araujo-Bazán 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 : 891905.[CrossRef]
153. Echauri-Espinosa RO,, Callejas-Negrete OA,, Roberson RW,, Bartnicki-García S,, Mouriño-Pérez RR . 2012. 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.[CrossRef]
154. Epp E,, Nazarova E,, Regan H,, Douglas LM,, Konopka JB,, Vogel J,, Whiteway M . 2013. Clathrin- and Arp2/3-independent endocytosis in the fungal pathogen Candida albicans . MBio 4 : e00476-13.[CrossRef]
155. Fuchs U,, Hause G,, Schuchardt I,, Steinberg G . 2006. Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis . Plant Cell 18 : 20662081.[CrossRef]
156. Higuchi Y,, Shoji JY,, Arioka M,, Kitamoto K . 2009. Endocytosis is crucial for cell polarity and apical membrane recycling in the filamentous fungus Aspergillus oryzae . Eukaryot Cell 8 : 3746.[CrossRef] [PubMed]
157. Jorde S,, Walther A,, Wendland J . 2011. The Ashbya gossypii fimbrin SAC6 is required for fast polarized hyphal tip growth and endocytosis. Microbiol Res 166 : 137145.[CrossRef] [PubMed]
158. Martin R,, Hellwig D,, Schaub Y,, Bauer J,, Walther A,, Wendland J . 2007. Functional analysis of Candida albicans genes whose Saccharomyces cerevisiae homologues are involved in endocytosis. Yeast 24 : 511522.[CrossRef]
159. Matsuo K,, Higuchi Y,, Kikuma T,, Arioka M,, Kitamoto K . 2013. Functional analysis of Abp1p-interacting proteins involved in endocytosis of the MCC component in Aspergillus oryzae . Fungal Genet Biol 56 : 125134.[CrossRef]
160. 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 : 19741986.[CrossRef] [PubMed]
161. Higuchi Y,, Ashwin P,, Roger Y,, Steinberg G . 2014. Early endosome motility spatially organizes polysome distribution. J Cell Biol 204 : 343357.[CrossRef]
162. Lemmon MA . 2003. Phosphoinositide recognition domains. Traffic 4 : 201213.[CrossRef]
163. Chavrier P,, Parton RG,, Hauri HP,, Simons K,, Zerial M . 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62 : 317329.[CrossRef] [PubMed]
164. van der Sluijs P,, Hull M,, Webster P,, Mâle P,, Goud B,, Mellman I . 1992. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70 : 729740.[CrossRef]
165. Seidel C,, Moreno-Velásquez SD,, Riquelme M,, Fischer R . 2013. Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot Cell 12 : 10201032.[CrossRef]
166. Kilaru S,, Schuster M,, Latz M,, Guo M,, Steinberg G . 2015. Fluorescent markers of the endocytic pathway in Zymoseptoria tritici . Fungal Genet Biol 79 : 150157.[CrossRef]
167. Egan MJ,, McClintock MA,, Reck-Peterson SL . 2012. Microtubule-based transport in filamentous fungi. Curr Opin Microbiol 15 : 637645.[CrossRef] [PubMed]
168. Svoboda K,, Schmidt CF,, Schnapp BJ,, Block SM . 1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365 : 721727.[CrossRef]
169. Toba S,, Watanabe TM,, Yamaguchi-Okimoto L,, Toyoshima YY,, Higuchi H . 2006. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc Natl Acad Sci USA 103 : 57415745.[CrossRef]
170. Plamann M,, Minke PF,, 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 : 139149.[CrossRef] [PubMed]
171. Xiang X,, Beckwith SM,, Morris NR . 1994. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans . Proc Natl Acad Sci USA 91 : 21002104.[CrossRef] [PubMed]
172. Steinberg G,, Schliwa M . 1995. The Neurospora organelle motor: a distant relative of conventional kinesin with unconventional properties. Mol Biol Cell 6 : 16051618.[CrossRef]
173. Wu Q,, Sandrock TM,, Turgeon BG,, Yoder OC,, Wirsel SG,, Aist JR . 1998. A fungal kinesin required for organelle motility, hyphal growth, and morphogenesis. Mol Biol Cell 9 : 89101.[CrossRef] [PubMed]
174. Steinberg G . 1997. A kinesin-like mechanoenzyme from the zygomycete Syncephalastrum racemosum shares biochemical similarities with conventional kinesin from Neurospora crassa . Eur J Cell Biol 73 : 124131.[PubMed]
175. Lenz JH,, Schuchardt I,, Straube A,, Steinberg G . 2006. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J 25 : 22752286.[CrossRef]
176. Zhang J,, Li S,, Fischer R,, Xiang X . 2003. Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 14 : 14791488.[CrossRef] [PubMed]
177. Steinberg G . 2011. Motors in fungal morphogenesis: cooperation versus competition. Curr Opin Microbiol 14 : 660667.[CrossRef] [PubMed]
178. Wedlich-Söldner R,, Straube A,, Friedrich MW,, Steinberg G . 2002. A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis . EMBO J 21 : 29462957.[CrossRef] [PubMed]
179. Egan MJ,, Tan K,, Reck-Peterson SL . 2012. Lis1 is an initiation factor for dynein-driven organelle transport. J Cell Biol 197 : 971982.[CrossRef] [PubMed]
180. Zekert N,, Fischer R . 2009. The Aspergillus nidulans kinesin-3 UncA motor moves vesicles along a subpopulation of microtubules. Mol Biol Cell 20 : 673684.[CrossRef] [PubMed]
181. Miki H,, Setou M,, Kaneshiro K,, Hirokawa N . 2001. All kinesin superfamily protein, KIF, genes in mouse and human. Proc Natl Acad Sci USA 98 : 70047011.[CrossRef]
182. Steinberg G,, Perez-Martin J . 2008. Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol 18 : 6167.[CrossRef] [PubMed]
183. Higuchi Y,, Nakahama T,, Shoji JY,, Arioka M,, Kitamoto K . 2006. Visualization of the endocytic pathway in the filamentous fungus Aspergillus oryzae using an EGFP-fused plasma membrane protein. Biochem Biophys Res Commun 340 : 784791.[CrossRef]
184. Han G,, Liu B,, Zhang J,, Zuo W,, Morris NR,, Xiang X . 2001. The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr Biol 11 : 719724.[CrossRef]
185. Schuster M,, Kilaru S,, Ashwin P,, Lin C,, Severs NJ,, Steinberg G . 2011. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J 30 : 652664.[CrossRef] [PubMed]
186. Schuster M,, Lipowsky R,, Assmann MA,, Lenz P,, Steinberg G . 2011. Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc Natl Acad Sci USA 108 : 36183623.[CrossRef]
187. Zhang J,, Qiu R,, Arst HN Jr,, Peñalva MA,, Xiang X . 2014. HookA is a novel dynein-early endosome linker critical for cargo movement in vivo . J Cell Biol 204 : 10091026.[CrossRef]
188. Bielska E,, Schuster M,, Roger Y,, Berepiki A,, Soanes DM,, Talbot NJ,, Steinberg G . 2014. Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes. J Cell Biol 204 : 9891007.[CrossRef]