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  • Review Article
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Actin organization and dynamics in filamentous fungi

Nature Reviews Microbiology volume 9, pages 876–887 (2011)Cite this article

Subjects

Key Points

  • The dynamic reorganization and polarization of the actin cytoskeleton underpins the growth and morphogenesis of filamentous fungi.

  • Actin has crucial roles in exocytosis, endocytosis, organelle movement and cytokinesis in fungi. These processes are coupled to the production of distinct higher-order structures (actin patches, cables and rings) that generate forces or serve as tracks for intracellular transport.

  • New approaches for imaging filamentous actin (F-actin) in living cells using the reporter Lifeact (an actin-binding peptide fused to GFP) have recently been developed for filamentous fungi. Live-cell imaging of F-actin, together with mutational studies, has yielded key insights into cell polarity, tip growth and long-distance transport.

  • F-actin organization and dynamics in filamentous fungi possess some features that have not been observed in Saccharomyces cerevisiae. For example, some actin patches exhibit bidirectional movement, actin cables can be long (5–20 μm), the polarized organization of actin in hyphal tips undergoes a radical change in organization during the transition from a germ tube to a mature vegetative hypha, and complex actin arrays show retrograde movement in germ tubes.

  • The concentration of F-actin in the core of the vesicle supply centre (the Spitzenkörper) within the tips of growing vegetative hyphae may represent a fourth type of higher-order structure, found in filamentous fungi but absent from S. cerevisiae. The precise roles of the Spitzenkörper remain to be elucidated.

Abstract

Growth and morphogenesis of filamentous fungi is underpinned by dynamic reorganization and polarization of the actin cytoskeleton. Actin has crucial roles in exocytosis, endocytosis, organelle movement and cytokinesis in fungi, and these processes are coupled to the production of distinct higher-order structures (actin patches, cables and rings) that generate forces or serve as tracks for intracellular transport. New approaches for imaging actin in living cells are revealing important similarities and differences in actin architecture and organization within the fungal kingdom, and have yielded key insights into cell polarity, tip growth and long-distance intracellular transport. In this Review, we discuss the contribution that recent live-cell imaging and mutational studies have made to our understanding of the dynamics and regulation of actin in filamentous fungi.

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Figure 1: Properties of actin and higher-order actin structures in filamentous fungi.
Figure 2: Model of actin-related protein 2/3 complex-mediated actin nucleation and actin patch transport in filamentous fungi.
Figure 3: Actin cable assembly and dynamics.
Figure 4: Rearrangement of the tip growth apparatus.
Figure 5: Model of contractile actomyosin ring assembly in Neurospora crassa.

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References

  1. May, G. S. & Adams, T. H. The importance of fungi to man. Genome Res. 7, 1041–1044 (1997).

    Article  CAS  PubMed  Google Scholar 

  2. Read, N. D. in Fungi and the Environment (eds Gadd, G. M., Watkinson, S. C. & Dyer, P. S.) 38–57 (Cambridge Univ. Press, Cambridge, UK, 2006).

    Google Scholar 

  3. Liu, Y. J. & Hall, B. D. Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc. Natl Acad. Sci. USA 101, 4507–4512 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bartnicki-Garcia, S. in Molecular Biology of Fungal Development (ed. Osiewaqcz, H. D.) 29–58 (Marcel Dekker, New York, 2002).

    Google Scholar 

  5. Bartnicki-Garcia, S., Bracker, C. E., Gierz, G., Lopez-Franco, R. & Lu, H. Mapping the growth of fungal hyphae: orthogonal cell wall expansion during tip growth and the role of turgor. Biophys. J. 79, 2382–2390 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lew, R. R. How does a hypha grow? The biophysics of pressurized growth in fungi. Nature Rev. Microbiol. 9, 509–518 (2011).

    Article  CAS  Google Scholar 

  7. Pruyne, D. W., Schott, D. H. & Bretscher, A. Tropomyosin-containing actin cables direct the Myo2p- dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143, 1931–1945 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Schott, D. H., Collins, R. N. & Bretscher, A. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156, 35–39 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Motegi, F., Arai, R. & Mabuchi, I. Identification of two type V myosins in fission yeast, one of which functions in polarized cell growth and moves rapidly in the cell. Mol. Biol. Cell 12, 1367–1380 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Harris, S. D. et al. Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryot. Cell 4, 225–229 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lichius, A., Berepiki, A. & Read, N. D. Form follows function – the versatile fungal cytoskeleton. Fungal Biol. 115, 518–540 (2011).

    Article  CAS  PubMed  Google Scholar 

  12. Knechtle, P., Wendland, J. & Philippsen, P. The SH3/PH domain protein AgBoi1/2 collaborates with the Rho-type GTPase AgRho3 to prevent nonpolar growth at hyphal tips of Ashbya gossypii. Eukaryot. Cell 5, 1635–1647 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Torralba, S., Raudaskoski, M., Pedregosa, A. M. & Laborda, F. Effect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology 144, 45–53 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Pantazopoulou, A. & Penalva, M. A. Organization and dynamics of the Aspergillus nidulans Golgi during apical extension and mitosis. Mol. Biol. Cell 20, 4335–4347 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Taheri-Talesh, N. et al. The tip growth apparatus of Aspergillus nidulans. Mol. Biol. Cell 19, 1439–1449 (2008). Live-cell analysis of hyphal-tip organization using a combination of markers for actin, endocytosis and exocytosis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Araujo-Bazan, L., Penalva, M. A. & Espeso, E. A. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol. Microbiol. 67, 891–905 (2008). The demonstration that endocytic components are polarized and form a subapical ring at hyphal tips.

    Article  CAS  PubMed  Google Scholar 

  17. Upadhyay, S. & Shaw, B. D. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol. Microbiol. 68, 690–705 (2008). An article that highlights the importance of endocytosis for correct polar growth and describes a subapical ring of endocytic components at hyphal tips.

    Article  CAS  PubMed  Google Scholar 

  18. Ayscough, K. R. et al. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin A. J. Cell Biol. 137, 399–416 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Barja, F., Chappuis, M. L. & Turian, G. Differential effects of anticytoskeletal compounds on the localization and chemical patterns of actin in germinating conidia of Neurospora crassa. FEMS Microbiol. Lett. 107, 261–266 (1993).

    Article  CAS  PubMed  Google Scholar 

  20. Harris, S. D., Morrell, J. L. & Hamer, J. E. Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136, 517–532 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Novick, P. & Botstein, D. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 40, 405–416 (1985).

    Article  CAS  PubMed  Google Scholar 

  22. Virag, A. & Griffiths, A. J. A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet. Biol. 41, 213–225 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. Rida, P. C. G., Nishikawa, A., Won, G. Y. & Dean, N. Yeast-to-hyphal transition triggers formin-dependent Golgi localization to the growing tip in Candida albicans. Mol. Biol. Cell 17, 4364–4378 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Suelmann, R. & Fischer, R. Mitochondrial movement and morphology depend on an intact actin cytoskeleton in Aspergillus nidulans. Cell Motil. Cytoskeleton 45, 42–50 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Dominguez, R. & Holmes, K. C. Actin structure and function. Annu. Rev. Biophys. 40, 169–186 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kovar, D. R., Sirotkin, V. & Lord, M. Three's company: the fission yeast actin cytoskeleton. Trends Cell Biol. 21, 177–187 (2011).

    Article  CAS  PubMed  Google Scholar 

  27. Moseley, J. B. & Goode, B. L. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70, 605–645 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Harris, S. D. & Momany, M. Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet. Biol. 41, 391–400 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Seiler, S. & Plamann, M. The genetic basis of cellular morphogenesis in the filamentous fungus Neurospora crassa. Mol. Biol. Cell 14, 4352–4364 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Berepiki, A., Lichius, A., Shoji, J. Y., Tilsner, J. & Read, N. D. F-actin dynamics in Neurospora crassa. Eukaryot. Cell 9, 547–557 (2010). The first study to use the Lifeact probe to provide detailed live-cell imaging of F-actin localization and dynamics in germlings and vegetative hyphae of N. crassa.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Delgado-Alvarez, D. L. et al. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet. Biol. 47, 573–586 (2010). An in-depth description of the localization of F-actin and various ABPs in hyphae of N. crassa.

    Article  CAS  PubMed  Google Scholar 

  32. Howard, R. J. Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze-substitution. J. Cell Sci. 48, 89–103 (1981). A classic paper providing the first description of the ultrastructural localization of actin in hyphal tips.

    CAS  PubMed  Google Scholar 

  33. Bourett, T. M. & Howard, R. J. Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163, 199–202 (1991).

    Article  Google Scholar 

  34. Roberson, R. W. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84, 41–51 (1992).

    Article  CAS  Google Scholar 

  35. Adams, A. E. & Pringle, J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J. Cell Biol. 98, 934–945 (1984).

    Article  CAS  PubMed  Google Scholar 

  36. Kilmartin, J. V. & Adams, A. E. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J. Cell Biol. 98, 922–933 (1984).

    Article  CAS  PubMed  Google Scholar 

  37. Marks, J., Hagan, I. M. & Hyams, J. S. Growth polarity and cytokinesis in fission yeast: the role of the cytoskeleton. J. Cell Sci. 5, 229–241 (1986).

    Article  CAS  Google Scholar 

  38. Yokoyama, K., Kaji, H., Nishimura, K. & Miyaji, M. The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans. J. Gen. Microbiol. 136, 1067–1075 (1990).

    Article  CAS  PubMed  Google Scholar 

  39. Garrill, A. & Suei, S. An F-actin-depleted zone is present at the hyphal tip of invasive hyphae of Neurospora crassa. Protoplasma 232, 165–172 (2008).

    Article  CAS  PubMed  Google Scholar 

  40. Barja, F., Thi, B. N. & Turian, G. Localization of actin and characterization of its isoforms in the hyphae of Neurospora crassa. FEMS Microbiol. Lett. 61, 19–24 (1991).

    Article  CAS  PubMed  Google Scholar 

  41. Kubler, E. & Riezman, H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 12, 2855–2862 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mulholland, J. et al. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125, 381–391 (1994).

    Article  CAS  PubMed  Google Scholar 

  43. Munn, A. L., Stevenson, B. J., Geli, M. I. & Riezman, H. End5, End6, and End7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6, 1721–1742 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Robertson, A. S., Smythe, E. & Ayscough, K. R. Functions of actin in endocytosis. Cell. Mol. Life Sci. 66, 2049–2065 (2009).

    Article  CAS  PubMed  Google Scholar 

  45. Huckaba, T. M., Gay, A. C., Pantalena, L. F., Yang, H. C. & Pon, L. A. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 167, 519–530 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Altschuler, S. J., Marco, E., Wedlich-Soldner, R., Li, R. & Wu, L. F. Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129, 411–422 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Penalva, M. A. Endocytosis in filamentous fungi: Cinderella gets her reward. Curr. Opin. Microbiol. 13, 684–692 (2010).

    Article  CAS  PubMed  Google Scholar 

  48. Steinberg, G. On the move: endosomes in fungal growth and pathogenicity. Nature Rev. Microbiol. 5, 309–316 (2007).

    Article  CAS  Google Scholar 

  49. Kaksonen, M., Sun, Y. & Drubin, D. G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115, 475–487 (2003). A landmark investigation showing that different types of patch behaviour are determined by the varying protein composition of actin patches.

    Article  CAS  PubMed  Google Scholar 

  50. Sanchez-Ferrero, J. C. & Peñalva, M. A. in The Aspergilli: Genomics, Medical Applications, Biotechnology, and Research Methods (eds Osmani, S. & Goldman, G.) 177–195 (CRC Press, Boca Raton, 2007).

    Book  Google Scholar 

  51. Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305–320 (2005).

    Article  CAS  PubMed  Google Scholar 

  52. Li, R. Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J. Cell Biol. 136, 649–658 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Madania, A. et al. The Saccharomyces cerevisiae homologue of human Wiskott–Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol. Biol. Cell 10, 3521–3538 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Jonsdottir, G. A. & Li, R. Dynamics of yeast myosin I: evidence for a possible role in scission of endocytic vesicles. Curr. Biol. 14, 1604–1609 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. Sun, Y. D., Martin, A. C. & Drubin, D. G. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev. Cell 11, 33–46 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. Ayscough, K. R. et al. Interactions between the yeast SM22 homologue Scp1 and actin demonstrate the importance of actin bundling in endocytosis. J. Biol. Chem. 283, 15037–15046 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Aghamohammadzadeh, S. & Ayscough, K. R. Differential requirements for actin during yeast and mammalian endocytosis. Nature Cell Biol. 11, 1039–1042 (2009).

    Article  CAS  PubMed  Google Scholar 

  58. Ayscough, K. R. Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton. Curr. Biol. 10, 1587–1590 (2000).

    Article  CAS  PubMed  Google Scholar 

  59. Walther, T. C. et al. Eisosomes mark static sites of endocytosis. Nature 439, 998–1003 (2006).

    Article  CAS  PubMed  Google Scholar 

  60. Grossman, G. et al. Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. 183, 1075–1088 (2008).

    Article  CAS  Google Scholar 

  61. Reijnst, P., Walther, A. & Wendland, J. Dual-colour fluorescence microscopy using yEmCherry-/GFP-tagging of eisosome components Pil1 and Lsp1 in Candida albicans. Yeast 28, 331–338 (2011).

    Article  CAS  PubMed  Google Scholar 

  62. Seger, S., Rischatsch, R. & Philippsen, P. Formation and stability of eisosomes in the filamentous fungus Ashbya gossypii. J. Cell Sci. 124, 1629–1634 (2011).

    Article  CAS  PubMed  Google Scholar 

  63. Vangelatos, I. et al. Eisosome organization in the filamentous ascomycete Aspergillus nidulans. Eukaryot. Cell 9, 1441–1454 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Borkovich, K. A. et al. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68, 1–108 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lees-Miller, J. P., Henry, G. & Helfman, D. M. Identification of Act2, an essential gene in the fission yeast Schizosaccharomyces pombe that encodes a protein related to actin. Proc. Natl Acad. Sci. USA 89, 80–83 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Roca, M. G., Kuo, H. C., Lichius, A., Freitag, M. & Read, N. D. Nuclear dynamics, mitosis, and the cytoskeleton during the early stages of colony initiation in Neurospora crassa. Eukaryot. Cell 9, 1171–1183 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Schwob, E. & Martin, R. P. New yeast actin-like gene required late in the cell cycle. Nature 355, 179–182 (1992).

    Article  CAS  PubMed  Google Scholar 

  68. Whiteway, M. et al. Forward genetics in Candida albicans that reveals the Arp2/3 complex is required for hyphal formation, but not endocytosis. Mol. Microbiol. 75, 1182–1198 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Martin, A. C. et al. Effects of Arp2 and Arp3 nucleotide-binding pocket mutations on Arp2/3 complex function. J. Cell Biol. 168, 315–328 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Robertson, A. S. et al. The WASP homologue Las17 activates the novel actin-regulatory activity of Ysc84 to promote endocytosis in yeast. Mol. Biol. Cell 20, 1618–1628 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pelham, R. J. Jr & Chang, F. Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nature Cell Biol. 3, 235–244 (2001).

    Article  CAS  PubMed  Google Scholar 

  72. Sirotkin, V., Berro, J., Macmillan, K., Zhao, L. & Pollard, T. D. Quantitative analysis of the mechanism of endocytic actin patch assembly and disassembly in fission yeast. Mol. Biol. Cell 21, 2894–2904 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Doyle, T. & Botstein, D. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl Acad. Sci. USA 93, 3886–3891 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Smith, M. G., Swamy, S. R. & Pon, L. A. The life cycle of actin patches in mating yeast. J. Cell Sci. 114, 1505–1513 (2001).

    CAS  PubMed  Google Scholar 

  75. Waddle, J. A., Karpova, T. S., Waterston, R. H. & Cooper, J. A. Movement of cortical actin patches in yeast. J. Cell Biol. 132, 861–870 (1996).

    Article  CAS  PubMed  Google Scholar 

  76. Abenza, J. F., Pantazopoulou, A., Rodriguez, J. M., Galindo, A. & Penalva, M. A. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10, 57–75 (2009).

    Article  CAS  PubMed  Google Scholar 

  77. Wedlich-Soldner, R., Bolker, M., Kahmann, R. & Steinberg, G. A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19, 1974–1986 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Jorde, S., Walther, A. & Wendland, J. The Ashbya gossypii fimbrin SAC6 is required for fast polarized hyphal tip growth and endocytosis. Microbiol. Res. 166, 137–145 (2011).

    Article  CAS  PubMed  Google Scholar 

  79. Higuchi, Y., Shoji, J. Y., Arioka, M. & Kitamoto, K. Endocytosis is crucial for cell polarity and apical membrane recycling in the filamentous fungus Aspergillus oryzae. Eukaryot. Cell 8, 37–46 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Hervas-Aguilar, A. & Penalva, M. A. Endocytic machinery protein SlaB is dispensable for polarity establishment but necessary for polarity maintenance in hyphal tip cells of Aspergillus nidulans. Eukaryot. Cell 9, 1504–1518 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Balguerie, A., Sivadon, P., Bonneu, M. & Aigle, M. Rvs167p, the budding yeast homolog of amphiphysin, colocalizes with actin patches. J. Cell Sci. 112, 2529–2537 (1999).

    CAS  PubMed  Google Scholar 

  82. Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499 (2004).

    Article  CAS  PubMed  Google Scholar 

  83. Konopka, J. B., Douglas, L. M. & Martin, S. W. BAR domain proteins Rvs161 and Rvs167 contribute to Candida albicans endocytosis, morphogenesis, and virulence. Infec. Immun. 77, 4150–4160 (2009).

    Article  CAS  Google Scholar 

  84. Walther, A. & Wendland, J. Polarized hyphal growth in Candida albicans requires the Wiskott-Aldrich syndrome protein homolog Wal1p. Eukaryot. Cell 3, 471–482 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Walther, A. & Wendland, J. Apical localization of actin patches and vacuolar dynamics in Ashbya gossypii depend on the WASP homolog Wal1p. J. Cell Sci. 117, 4947–4958 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Oberholzer, U., Marcil, A., Leberer, E., Thomas, D. Y. & Whiteway, M. Myosin I is required for hypha formation in Candida albicans. Eukaryot. Cell 1, 213–228 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Osherov, N., Yamashita, R. A., Chung, Y. S. & May, G. S. Structural requirements for in vivo myosin I function in Aspergillus nidulans. J. Biol. Chem. 273, 27017–27025 (1998).

    Article  CAS  PubMed  Google Scholar 

  88. Yamashita, R. A., Osherov, N. & May, G. S. Localization of wild type and mutant class I myosin proteins in Aspergillus nidulans using GFP-fusion proteins. Cell Motil. Cytoskeleton 45, 163–172 (2000).

    Article  CAS  PubMed  Google Scholar 

  89. Yamashita, R. A. & May, G. S. Constitutive activation of endocytosis by mutation of myoA, the myosin I gene of Aspergillus nidulans. J. Biol. Chem. 273, 14644–14648 (1998).

    Article  CAS  PubMed  Google Scholar 

  90. Evangelista, M., Pruyne, D., Amberg, D. C., Boone, C. & Bretscher, A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biol. 4, 260–269 (2002).

    Article  CAS  PubMed  Google Scholar 

  91. Pruyne, D. et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615 (2002).

    Article  CAS  PubMed  Google Scholar 

  92. Fehrenbacher, K. L., Boldogh, I. R. & Pon, L. A. Taking the A-train: actin-based force generators and organelle targeting. Trends Cell Biol. 13, 472–477 (2003).

    Article  CAS  PubMed  Google Scholar 

  93. Rossanese, O. W. et al. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 153, 47–62 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Hubbard, M. A. & Kaminskyj, S. G. Rapid tip-directed movement of Golgi equivalents in growing Aspergillus nidulans hyphae suggests a mechanism for delivery of growth-related materials. Microbiology 154, 1544–1553 (2008).

    Article  CAS  PubMed  Google Scholar 

  95. Fuchs, F., Prokisch, H., Neupert, W. & Westermann, B. Interaction of mitochondria with microtubules in the filamentous fungus Neurospora crassa. J. Cell Sci. 115, 1931–1937 (2002).

    CAS  PubMed  Google Scholar 

  96. Harris, S. D. Cdc42/Rho GTPases in fungi: variations on a common theme. Mol. Microbiol. 79, 1123–1127 (2011).

    Article  CAS  PubMed  Google Scholar 

  97. Kwon, M. J. et al. Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol. Microbiol. 79, 1151–1167 (2011).

    Article  CAS  PubMed  Google Scholar 

  98. Rasmussen, C. G. & Glass, N. L. A Rho-type GTPase, rho-4, is required for septation in Neurospora crassa. Eukaryot. Cell 4, 1913–1925 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Rasmussen, C. G. & Glass, N. L. Localization of RHO-4 indicates differential regulation of conidial versus vegetative septation in the filamentous fungus Neurospora crassa. Eukaryot. Cell 6, 1097–1107 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Mahlert, M., Leveleki, L., Hlubek, A., Sandrock, B. & Bolker, M. Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 59, 567–578 (2006).

    Article  CAS  PubMed  Google Scholar 

  101. Rolke, Y. & Tudzynski, P. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol. Microbiol. 68, 405–423 (2008).

    Article  CAS  PubMed  Google Scholar 

  102. Boyce, K. J., Hynes, M. J. & Andrianopoulos, A. Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J. Cell Sci. 116, 1249–1260 (2003).

    Article  CAS  PubMed  Google Scholar 

  103. Virag, A., Lee, M. P., Si, H. & Harris, S. D. Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol. Microbiol. 66, 1579–1596 (2007).

    CAS  PubMed  Google Scholar 

  104. Evangelista, M. et al. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118–122 (1997).

    Article  CAS  PubMed  Google Scholar 

  105. Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113, 365–375 (2000).

    CAS  PubMed  Google Scholar 

  106. Chesarone, M. A., DuPage, A. G. & Goode, B. L. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nature Rev. Mol. Cell Biol. 11, 62–74 (2010).

    Article  CAS  Google Scholar 

  107. Kovar, D. R., Kuhn, J. R., Tichy, A. L. & Pollard, T. D. The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J. Cell Biol. 161, 875–887 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Sagot, I., Klee, S. K. & Pellman, D. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nature Cell Biol. 4, 42–50 (2002).

    Article  CAS  PubMed  Google Scholar 

  109. Zigmond, S. H. et al. Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13, 1820–1823 (2003).

    Article  CAS  PubMed  Google Scholar 

  110. Moseley, J. B. et al. A conserved mechanism for Bni1-and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell 15, 896–907 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Chang, F., Drubin, D. & Nurse, P. Cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137, 169–182 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Kovar, D. R., Wu, J. Q. & Pollard, T. D. Profilin-mediated competition between capping protein and formin Cdc12p during cytokinesis in fission yeast. Mol. Biol. Cell 16, 2313–2324 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Kemper, M. et al. A Bnr-like formin links actin to the spindle pole body during sporulation in the filamentous fungus Ashbya gossypii. Mol. Microbiol. 80, 1276–1295 (2011). This study demonstrates that Bnr2 has an important role in sporulation and that during sporulation it assembles actin cables from the nuclear spindle pole body.

    Article  CAS  PubMed  Google Scholar 

  114. Schmitz, H. P., Kaufmann, A., Kohli, M., Laissue, P. P. & Philippsen, P. From function to shape: a novel role of a formin in morphogenesis of the fungus Ashbya gossypii. Mol. Biol. Cell 17, 130–145 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Harris, S. D., Hamer, L., Sharpless, K. E. & Hamer, J. E. The Aspergillus nidulans sepA gene encodes an FH1/2 protein involved in cytokinesis and the maintenance of cellular polarity. EMBO J. 16, 3474–3483 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Sharpless, K. E. & Harris, S. D. Functional characterization and localization of the Aspergillus nidulans formin SEPA. Mol. Biol. Cell 13, 469–479 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Justa-Schuch, D., Heilig, Y., Richthammer, C. & Seiler, S. 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, 220–235 (2010). A detailed study analysing the role of RHO-4 and BUD-4 during cytokinesis in N. crassa , and establishing the contribution of the activators BUD-3 and RGF-3 to this process.

    Article  CAS  PubMed  Google Scholar 

  118. Li, C. R. et al. The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J. Cell Sci. 118, 2637–2648 (2005).

    Article  CAS  PubMed  Google Scholar 

  119. Martin, R., Walther, A. & Wendland, H. Ras1-induced hyphal development in Candida albicans requires the formin Bni1. Eukaryot. Cell 4, 1712–1724 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Harispe, L., Portela, C., Scazzocchio, C., Penalva, M. A. & Gorfinkiel, L. Ras GTPase-activating protein regulation of actin cytoskeleton and hyphal polarity in Aspergillus nidulans. Eukaryot. Cell 7, 141–153 (2008).

    Article  CAS  PubMed  Google Scholar 

  121. Pearson, C. L., Xu, K. M., Sharpless, K. E. & Harris, S. D. MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans. Mol. Biol. Cell 15, 3658–3672 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Ren, B. et al. Genome-wide location and function of DNA binding proteins. Science 290, 2306–2309 (2000).

    Article  CAS  PubMed  Google Scholar 

  123. Yang, H. C. & Pon, L. A. Actin cable dynamics in budding yeast. Proc. Natl Acad. Sci. USA 99, 751–756 (2002). A seminal live-cell-imaging paper providing the first details of actin cable dynamics in S. cerevisiae.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Weber, I., Gruber, C. & Steinberg, G. A class-V myosin required for mating, hyphal growth, and pathogenicity in the dimorphic plant pathogen Ustilago maydis. Plant Cell 15, 2826–2842 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Woo, M., Lee, K. & Song, K. MYO2 is not essential for viability, but is required for polarized growth and dimorphic switches in Candida albicans. FEMS Microbiol. Lett. 218, 195–202 (2003).

    Article  CAS  PubMed  Google Scholar 

  126. Köhli, M., Galati, V., Boudier, K., Roberson, R. W. & Philippsen, P. Growth-speed-correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. J. Cell Sci. 121, 3878–3889 (2008). A comprehensive quantitative study showing that localization of the polarisome and exocyst is correlated with growth rate.

    Article  CAS  PubMed  Google Scholar 

  127. Ayad-Durieux, Y., Knechtle, P., Goff, S., Dietrich, F. & Philippsen, P. A PAK-like protein kinase is required for maturation of young hyphae and septation in the filamentous ascomycete Ashbya gossypii. J. Cell Sci. 113, 4563–4575 (2000).

    CAS  PubMed  Google Scholar 

  128. Knechtle, P., Kaufmann, A., Cavicchioli, D. & Philippsen, P. The Paxillin-like protein AgPxl1 is required for apical branching and maximal hyphal growth in Ashbya gossypii. Fungal Genet. Biol. 45, 829–838 (2008).

    Article  CAS  PubMed  Google Scholar 

  129. Araujo-Palomares, C. L., Riquelme, M. & Castro-Longoria, E. The polarisome component SPA-2 localizes at the apex of Neurospora crassa and partially colocalizes with the Spitzenkörper. Fungal Genet. Biol. 46, 551–563 (2009).

    Article  CAS  PubMed  Google Scholar 

  130. Virag, A. & Harris, S. D. Functional characterization of Aspergillus nidulans homologues of Saccharomyces cerevisiae Spa2 and Bud6. Eukaryot. Cell 5, 881–895 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Jones, L. A. & Sudbery, P. E. Spitzenkörper, exocyst, and polarisome components in Candida albicans hyphae show different patterns of localization and have distinct dynamic properties. Eukaryot. Cell 9, 1455–1465 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Pollard, T. D. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50–56 (2010).

    Article  CAS  PubMed  Google Scholar 

  133. Seiler, S. & Justa-Schuch, D. Conserved components, but distinct mechanisms for the placement and assembly of the cell division machinery in unicellular and filamentous ascomycetes. Mol. Microbiol. 78, 1058–1076 (2010).

    Article  CAS  PubMed  Google Scholar 

  134. Si, H., Justa-Schuch, D., Seiler, S. & Harris, S. D. Regulation of septum formation by the Bud3–Rho4 GTPase module in Aspergillus nidulans. Genetics 185, 165–176 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Wang, J. et al. The important role of actinin-like protein (AcnA) in cytokinesis and apical dominance of hyphal cells in Aspergillus nidulans. Microbiology 155, 2714–2725 (2009).

    Article  CAS  PubMed  Google Scholar 

  136. Lord, M., Laves, E. & Pollard, T. D. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol. Biol. Cell 16, 5346–5355 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Vavylonis, D., Wu, J. Q., Hao, S., O'Shaughnessy, B. & Pollard, T. D. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319, 97–100 (2008).

    Article  CAS  PubMed  Google Scholar 

  138. Wu, J. Q. & Pollard, T. D. Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310–314 (2005).

    Article  CAS  PubMed  Google Scholar 

  139. Pollard, T. D. et al. Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 174, 391–402 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Wu, J. Q., Coffman, V. C., Nile, A. H., Lee, I. J. & Liu, H. Y. Roles of formin nodes and myosin motor activity in Mid1p-dependent contractile-ring assembly during fission yeast cytokinesis. Mol. Biol. Cell 20, 5195–5210 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Oliferenko, S. & Mishra, M. Cytokinesis: catch and drag. Curr. Biol. 18, R247–R250 (2008).

    Article  CAS  PubMed  Google Scholar 

  142. Kreis, T. E., Winterhalter, K. H. & Birchmeier, W. In vivo distribution and turnover of fluorescently labeled actin microinjected into human fibroblasts. Proc. Natl Acad. Sci. USA 76, 3814–3818 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Wehland, J. & Weber, K. Actin rearrangement in living cells revealed by microinjection of a fluorescent phalloidin derivative. Eur. J. Cell Biol. 24, 176–183 (1981).

    CAS  PubMed  Google Scholar 

  144. Cooper, J. A. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105, 1473–1478 (1987).

    Article  CAS  PubMed  Google Scholar 

  145. Riedl, J. et al. Lifeact: a versatile marker to visualize F-actin. Nature Methods 5, 605–607 (2008). An outstanding report showing that F-actin can be visualized in a range of cell types using a 17 amino acid peptide (Lifeact) without any deleterious effects.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Riedl, J. et al. Lifeact mice for studying F-actin dynamics. Nature Methods 7, 168–169 (2010).

    Article  CAS  PubMed  Google Scholar 

  147. Ueda, T. et al. Application of Lifeact reveals F-actin dynamics in Arabidopsis thaliana and the liverwort, Marchantia polymorpha. Plant Cell Physiol. 50, 1041–1048 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Vidali, L., Rounds, C. M., Hepler, P. K. & Bezanilla, M. Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONE 4, e5744 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Girbardt, M. Der Spitzenkörper von Polysticus versicolor. Planta 50, 47–59 (1957).

    Article  Google Scholar 

  150. Verdin, J., Bartnicki-Garcia, S. & Riquelme, M. Functional stratification of the Spitzenkörper of Neurospora crassa. Mol. Microbiol. 74, 1044–1053 (2009).

    Article  CAS  PubMed  Google Scholar 

  151. Bracker, C. E., Murphy, D. J. & Lopez-Franco, R. in Functional Imaging of Optical Manipulation of Living Cells. Proceedings of SPIE., Vol. 2983 (eds Farkas, D. L. & Tromberg, B. J.) 67–80 (International Society of Optical Engineering, Bellingham, Washington, 1997).

    Book  Google Scholar 

  152. Bartnicki-Garcia, S., Hergert, F. & Gierz, G. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153, 46–57 (1989).

    Article  Google Scholar 

  153. Riquelme, M., Reynaga-Pena, C. G., Gierz, G. & Bartnicki-Garcia, S. What determines growth direction in fungal hyphae? Fungal Genet. Biol. 24, 101–109 (1998).

    Article  CAS  PubMed  Google Scholar 

  154. Steinberg, G. Hyphal growth: a tale of motors, lipids, and the Spitzenkörper. Eukaryot. Cell 6, 351–360 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Freitag, M., Hickey, P. C., Raju, N. B., Selker, E. U. & Read, N. D. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41, 897–910 (2004).

    Article  CAS  PubMed  Google Scholar 

  156. Takeshita, N., Higashitsuji, Y., Konzack, S. & Fischer, R. 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, 339–351 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Martin, S. G., McDonald, W. H., Yates, J. R. & Chang, F. Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev. Cell 8, 479–491 (2005).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by funding from the UK Biotechnological and Biological Sciences Research Council (BBSRC) (grant BB/E010741/1) to N.D.R., a Ph.D. Studentship from The University of Edinburgh to A.L. and a BBSRC Studentship to A.B. The authors also thank the Mexican National Council for Science and Technology (CONACyT) for a postdoctoral fellowship to A.L.

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  1. Fungal Cell Biology Group, Institute of Cell Biology, Rutherford Building, University of Edinburgh, Edinburgh, EH9 3JH, UK

    Adokiye Berepiki, Alexander Lichius & Nick D. Read

  2. Department of Microbiology, Center for Scientific Research and Higher Education of Ensenada (CICESE), Ensenada, 22860, Baja California, Mexico

    Alexander Lichius

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  1. Adokiye Berepiki
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Glossary

Microtubules

Tubular cytoskeletal polymers composed of tubulin dimers. They provide tracks for intracellular transport based on motor proteins (kinesin or dynein) and form the spindle apparatus that allows chromosome segregation during nuclear division.

Filasomes

Vesicles coated in filamentous actin.

Phalloidin

A toxin that binds specifically to the interface between filamentous actin (F-actin) subunits. Phalloidin conjugated to fluorescent dyes has been widely used for imaging F-actin in eukaryotic cells such as Saccharomyces cerevisiae but has not proved useful for staining F-actin in many filamentous fungi.

Clathrin

A structural protein that forms a cage-like, polyhedral molecular arrangement (a triskelion) composed of three heavy chains and three light chains. Clathrin shapes and coats vesicles during their formation.

Wiscott–Aldrich syndrome protein

(WASP). Founding member of a family of activators of the actin-related protein 2/3 (Arp2/3) complex that participate in signal transduction to the actin cytoskeleton.

Myosin

A superfamily of motor proteins that bind to microfilaments and couple ATP hydrolysis to force generation. Class I myosins are monomeric and are involved in endocytosis. Class II myosins are dimeric and can form filaments, which is important for their conserved role in cytokinesis. Class V myosins are dimeric processive motors that translocate cargoes along actin cables.

Fimbrin

A conserved actin-crosslinking protein that contains a conserved 100 amino acid calponin homology domain found in many actin-binding proteins.

FM4-64

A vital, membrane-selective, amphiphilic styryl dye commonly used to study endocytosis, vesicle trafficking, and organelle organization and movement in living fungal cells.

Lucifer yellow

A vital fluorescent dye used as a marker for fluid-phase endocytosis.

Formins

Large protein dimers that nucleate the formation of filamentous actin by the processive addition of globular actin to the barbed ends of actin microfilaments.

Tropomyosin

An actin-binding protein that binds to and stabilises filamentous actin, promoting actin cable formation.

Golgi equivalents

Single Golgi cisternae that are produced by most filamentous fungi instead of the stacks of cisternae found in animal and plant cells. These organelles process and package macromolecules that are destined for secretion.

Conidial anastomosis tubes

Specialized cell protrusions or short hyphae that emerge from asexual fungal spores (conidia) and mediate cell fusion during colony initiation.

Paxillin

An adaptor protein that participates in signal transduction and actin reorganization in mammalian cells.

Epistatic

Pertaining to a gene: masking the phenotypic effect of another gene.

Exocyst

A multiprotein complex involved in determining where vesicles dock and fuse with the plasma membrane.

Anillin

A Drosophila melanogaster scaffold protein that interacts with and organizes structural components of the contractile actin ring. Other eukaryotes encode anillin-related proteins with similar functions.

Actinin

An actin-binding protein that crosslinks filamentous actin and associates with the plasma membrane.

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Berepiki, A., Lichius, A. & Read, N. Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9, 876–887 (2011). https://doi.org/10.1038/nrmicro2666

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