1887

Abstract

Septins are a conserved family of GTP-binding proteins that are distributed across different lineages of the eukaryotes, with the exception of plants. Septins perform a myriad of functions in fungal cells, ranging from controlling morphogenetic events to contributing to host tissue invasion and virulence. One key attribute of the septins is their ability to assemble into heterooligomeric complexes that organizse into higher order structures. In addition to the established role of septins in the model budding yeast, , their importance in other fungi recently emerges. While newer roles for septins are being uncovered in these fungi, the mechanism of how septins assemble into a complex and their regulation is only beginning to be comprehended. In this review, we summarize recent findings on the role of septins in different fungi and focus on how the septin complexes of different fungi are organized and . Furthermore, we discuss on how phosphorylation/dephosphorylation can serve as an important mechanism of septin complex assembly and regulation.

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2016-09-01
2020-01-22
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References

  1. Alvarez-Tabarés I., Pérez-Martín J.. 2010; Septins from the phytopathogenic fungus Ustilago maydis are required for proper morphogenesis but dispensable for virulence. PLoS One5:e12933 [CrossRef][PubMed]
    [Google Scholar]
  2. Asano S., Park J. E., Yu L. R., Zhou M., Sakchaisri K., Park C. J., Kang Y. H., Thorner J., Veenstra T. D. et al. 2006; Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J Biol Chem281:27090–27098 [CrossRef][PubMed]
    [Google Scholar]
  3. Au Yong J. Y., Wang Y. M., Wang Y.. 2016; The Nim1 kinase Gin4 has distinct domains crucial for septin assembly, phospholipid binding and mitotic exit. J Cell Sci129:2744–2756 [CrossRef][PubMed]
    [Google Scholar]
  4. Badrane H., Nguyen M. H., Blankenship J. R., Cheng S., Hao B., Mitchell A. P., Clancy C. J.. 2012; Rapid redistribution of phosphatidylinositol-(4,5)-bisphosphate and septins during the Candida albicans response to caspofungin. Antimicrob Agents Chemother56:4614–4624 [CrossRef][PubMed]
    [Google Scholar]
  5. Barral Y., Parra M., Bidlingmaier S., Snyder M.. 1999; Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev13:176–187 [CrossRef]
    [Google Scholar]
  6. Berepiki A., Read N. D.. 2013; Septins are important for cell polarity, septation and asexual spore formation in Neurospora crassa and show different patterns of localisation at germ tube tips. PLoS One8:e63843 [CrossRef][PubMed]
    [Google Scholar]
  7. Bertin A., McMurray M. A., Grob P., Park S. S., Garcia G., Patanwala I., Ng H. L., Alber T., Thorner J. et al. 2008; Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci U S A105:8274–8279 [CrossRef][PubMed]
    [Google Scholar]
  8. Bertin A., McMurray M. A., Pierson J., Thai L., McDonald K. L., Zehr E. A., García G., Peters P., Thorner J. et al. 2012; Three-dimensional ultrastructure of the septin filament network in Saccharomyces cerevisiae . Mol Biol Cell23:423–432 [CrossRef][PubMed]
    [Google Scholar]
  9. Blankenship J. R., Fanning S., Hamaker J. J., Mitchell A. P.. 2010; An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog6:e1000752 [CrossRef][PubMed]
    [Google Scholar]
  10. Blankenship J. R., Cheng S., Woolford C. A., Xu W., Johnson T. M., Rogers P. D., Fanning S., Nguyen M. H., Clancy C. J., Mitchell A. P.. 2014; Mutational analysis of essential septins reveals a role for septin-mediated signaling in filamentation. Eukaryot . Cell13:1403–1410
    [Google Scholar]
  11. Boyce K. J., Chang H., D'Souza C. A., Kronstad J. W.. 2005; An Ustilago maydis septin is required for filamentous growth in culture and for full symptom development on maize. Eukaryot C ell 4:2044–2056[CrossRef]
    [Google Scholar]
  12. Bridges A. A., Zhang H., Mehta S. B., Occhipinti P., Tani T., Gladfelter A. S.. 2014; Septin assemblies form by diffusion-driven annealing on membranes. Proc Natl Acad Sci U S A111:2146–2151 [CrossRef][PubMed]
    [Google Scholar]
  13. Bridges A. A., Jentzsch M. S., Oakes P. W., Occhipinti P., Gladfelter A. S.. 2016; Micron-scale plasma membrane curvature is recognized by the septin cytoskeleton. J Cell Biol213:23–32 [CrossRef][PubMed]
    [Google Scholar]
  14. Caviston J. P., Longtine M., Pringle J. R., Bi E.. 2003; The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol Biol Cell14:4051–4066 [CrossRef][PubMed]
    [Google Scholar]
  15. Chao J. T., Wong A. K., Tavassoli S., Young B. P., Chruscicki A., Fang N. N., Howe L. J., Mayor T., Foster L. J. et al. 2014; Polarization of the endoplasmic reticulum by ER-septin tethering. Cell158:620–632 [CrossRef][PubMed]
    [Google Scholar]
  16. Chen A., Xie Q., Lin Y., Xu H., Shang W., Zhang J., Zhang D., Zheng W., Li G. et al. 2016; Septins are involved in nuclear division, morphogenesis and pathogenicity in Fusarium graminearum . Fungal Genet Biol94:79–87 [CrossRef][PubMed]
    [Google Scholar]
  17. Chi A., Huttenhower C., Geer L. Y., Coon J. J., Syka J. E. P., Bai D. L., Shabanowitz J., Burke D. J., Troyanskaya O. G. et al. 2007; Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc Natl Acad Sci U S A104:2193–2198 [CrossRef]
    [Google Scholar]
  18. Cvrcková F., De Virgilio C., Manser E., Pringle J. R., Nasmyth K.. 1995; Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast. Genes Dev9:1817–1830 [CrossRef][PubMed]
    [Google Scholar]
  19. Dagdas Y. F., Yoshino K., Dagdas G., Ryder L. S., Bielska E., Steinberg G., Talbot N. J.. 2012; Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae . Science336:1590–1595 [CrossRef][PubMed]
    [Google Scholar]
  20. DeMarini D. J., Adams A. E., Fares H., De Virgilio C., Valle G., Chuang J. S., Pringle J. R.. 1997; A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J Cell Biol139:1 [CrossRef][PubMed]
    [Google Scholar]
  21. DeMay B. S., Meseroll R. A., Occhipinti P., Gladfelter A. S.. 2009; Regulation of distinct septin rings in a single cell by Elm1p and Gin4p kinases. Mol Biol Cell20:2311–2326 [CrossRef][PubMed]
    [Google Scholar]
  22. Dobbelaere J., Gentry M. S., Hallberg R. L., Barral Y.. 2003; Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell4:345–357 [CrossRef][PubMed]
    [Google Scholar]
  23. Fares H., Goetsch L., Pringle J. R.. 1996; Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae . J Cell Biol132:399–411 [CrossRef][PubMed]
    [Google Scholar]
  24. Ficarro S. B., McCleland M. L., Stukenberg P. T., Burke D. J., Ross M. M., Shabanowitz J., Hunt D. F., White F. M.. 2002; Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae . Nat Biotechnol20:301–305 [CrossRef][PubMed]
    [Google Scholar]
  25. Garcia G. 3rd, Bertin A., Li Z., Song Y., McMurray M. A., Thorner J., Nogales E.. 2011; Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J Cell Biol195:993–1004 [CrossRef][PubMed]
    [Google Scholar]
  26. Gladfelter A. S., Pringle J. R., Lew D. J.. 2001; The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol4:681–689 [CrossRef][PubMed]
    [Google Scholar]
  27. Gladfelter A. S., Bose I., Zyla T. R., Bardes E. S., Lew D. J.. 2002; Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J Cell Biol156:315–326 [CrossRef][PubMed]
    [Google Scholar]
  28. González-Novo A., Correa-Bordes J., Labrador L., Sánchez M., Vázquez de Aldana C. R., Jiménez J.. 2008; Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol Biol Cell19:1509–1518 [CrossRef][PubMed]
    [Google Scholar]
  29. Hall P. A., Jung K., Hillan K. J., Russell S. E.. 2005; Expression profiling the human septin gene family. J Pathol206:269–278 [CrossRef][PubMed]
    [Google Scholar]
  30. Hartwell L. H.. 1971; Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res69:265–276 [CrossRef][PubMed]
    [Google Scholar]
  31. Heasley L. R., McMurray M. A.. 2016; Roles of septins in prospore membrane morphogenesis and spore wall assembly in Saccharomyces cerevisiae . Mol Biol Cell27:442–450 [CrossRef][PubMed]
    [Google Scholar]
  32. Helfer H., Gladfelter A. S.. 2006; AgSwe1p regulates mitosis in response to morphogenesis and nutrients in multinucleated Ashbya gossypii cells. Mol Biol Cell17:4494–4512 [CrossRef][PubMed]
    [Google Scholar]
  33. Hernandez-Rodriguez Y., Hastings S., Momany M.. 2012; The septin AspB in Aspergillus nidulans forms bars and filaments and plays roles in growth emergence and conidiation. Eukaryot Cell 11:311–323[CrossRef]
    [Google Scholar]
  34. Hernández-Rodríguez Y., Masuo S., Johnson D., Orlando R., Smith A., Couto-Rodriguez M., Momany M.. 2014; Distinct septin heteropolymers co-exist during multicellular development in the filamentous fungus Aspergillus nidulans . PLoS One9:e92819 [CrossRef][PubMed]
    [Google Scholar]
  35. Iwase M., Luo J., Nagaraj S., Longtine M., Kim H. B., Haarer B. K., Caruso C., Tong Z., Pringle J. R. et al. 2006; Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol Biol Cell17:1110–1125 [CrossRef][PubMed]
    [Google Scholar]
  36. Juvvadi P. R., Fortwendel J. R., Rogg L. E., Steinbach W. J.. 2011; Differential localization patterns of septins during growth of the human fungal pathogen Aspergillus fumigatus reveal novel functions. Biochem Biophys Res Commun405:238–243 [CrossRef][PubMed]
    [Google Scholar]
  37. Juvvadi P. R., Belina D., Soderblom E. J., Moseley M. A., Steinbach W. J.. 2013; Filamentous fungal-specific septin AspE is phosphorylated in vivo and interacts with actin, tubulin and other septins in the human pathogen Aspergillus fumigatus . Biochem Biophys Res Commun431:547–553 [CrossRef][PubMed]
    [Google Scholar]
  38. Kadota J., Yamamoto T., Yoshiuchi S., Bi E., Tanaka K.. 2004; Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae . Mol Biol Cell15:5329–5345 [CrossRef][PubMed]
    [Google Scholar]
  39. Khan A., McQuilken M., Gladfelter A. S.. 2015; Septins and generation of asymmetries in fungal cells. Annu Rev Microbiol69:487–503 [CrossRef][PubMed]
    [Google Scholar]
  40. Kim H. B., Haarer B. K., Pringle J. R.. 1991; Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. J Cell Biol112:535–544 [CrossRef][PubMed]
    [Google Scholar]
  41. Kozubowski L., Heitman J.. 2010; Septins enforce morphogenetic events during sexual reproduction and contribute to virulence of Cryptococcus neoformans . Mol Microbiol75:658–675 [CrossRef][PubMed]
    [Google Scholar]
  42. Li C.-R., Yong J.-Y. A., Wang Y.-M., Wang Y.. 2012a; CDK regulates septin organization through cell-cycle-dependent phosphorylation of the Nim1-related kinase Gin4. J Cell Sci125:2533–2543 [CrossRef]
    [Google Scholar]
  43. Li L., Zhang C., Konopka J. B.. 2012b; A Candida albicans temperature-sensitive cdc12-6 mutant identifies roles for septins in selection of sites of germ tube formation and hyphal morphogenesis. Eukaryot Cell11:1210–1218[CrossRef]
    [Google Scholar]
  44. Lindsey R., Cowden S., Hernandez-Rodriguez Y., Momany M.. 2010a; Septins AspA and AspC are important for normal development and limit the emergence of new growth foci in the multicellular fungus Aspergillus nidulans . Eukaryot Cell9:155–163[CrossRef]
    [Google Scholar]
  45. Lindsey R., Ha Y., Momany M.. 2010b; A septin from the filamentousfungus A. nidulans induces atypicalpseudohyphae in the budding yeast S.cerevisiae . PLoS One5:e9858 [CrossRef]
    [Google Scholar]
  46. Liu Q., Han Q., Wang N., Yao G., Zeng G., Wang Y., Huang Z., Sang J., Wang Y.. 2016; Tpd3-Pph21 phosphatase plays a direct role in Sep7 dephosphorylation in Candida albicans . Mol Microbiol101:109–121 [CrossRef][PubMed]
    [Google Scholar]
  47. Longtine M. S., Fares H., Pringle J. R.. 1998; Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J Cell Biol143:719–736 [CrossRef][PubMed]
    [Google Scholar]
  48. McMurray M. A., Thorner J.. 2009; Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div4:18 [CrossRef][PubMed]
    [Google Scholar]
  49. Meseroll R. A., Howard L., Gladfelter A. S.. 2012; Septin ring size scaling and dynamics require the coiled-coil region of Shs1p. Mol Biol Cell23:3391–3406 [CrossRef][PubMed]
    [Google Scholar]
  50. Meseroll R. A., Occhipinti P., Gladfelter A. S.. 2013; Septin phosphorylation and coiled-coil domains function in cell and septin ring morphology in the filamentous fungus Ashbya gossypii . Eukaryot Cell 12:182–193 [CrossRef][PubMed]
    [Google Scholar]
  51. Momany M., Zhao J., Lindsey R., Westfall P. J.. 2001; Characterization of the Aspergillus nidulans septin (asp) gene family. Genetics157:969–977[PubMed]
    [Google Scholar]
  52. Morrell J. L., Nichols C. B., Gould K. L.. 2004; The GIN4 family kinase, Cdr2p, acts independently of septins in fission yeast. J Cell Sci117:5293–5302 [CrossRef]
    [Google Scholar]
  53. Mortensen E. M., McDonald H., Yates J., Kellogg D. R.. 2002; Cell cycle-dependent assembly of a Gin4-septin complex. Mol Biol Cell13:2091–2105 [CrossRef][PubMed]
    [Google Scholar]
  54. Nguyen T. Q., Sawa H., Okano H., White J. G.. 2000; The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. J Cell Sci113:3825–3837[PubMed]
    [Google Scholar]
  55. Nishihama R., Onishi M., Pringle J. R.. 2011; New insights into the phylogenetic distribution and evolutionary origins of the septins. Biol Chem392:681–687 [CrossRef][PubMed]
    [Google Scholar]
  56. Oh Y., Bi E.. 2011; Septin structure and function in yeast and beyond. Trends Cell Biol21:141–148 [CrossRef][PubMed]
    [Google Scholar]
  57. Pan F., Malmberg R. L., Momany M.. 2007; Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol Biol7:103 [CrossRef][PubMed]
    [Google Scholar]
  58. Renz C., Oeljeklaus S., Grinhagens S., Warscheid B., Johnsson N., Gronemeyer T.. 2016; Identification of cell cycle dependent interaction partners of the septins by quantitative mass spectrometry. PLoS One11:e0148340 [CrossRef][PubMed]
    [Google Scholar]
  59. Roelants F. M., Su B. M., von Wulffen J., Ramachandran S., Sartorel E., Trott A. E., Thorner J.. 2015; Protein kinase Gin4 negatively regulates flippase function and controls plasma membrane asymmetry. J Cell Biol208:299–311 [CrossRef][PubMed]
    [Google Scholar]
  60. Sadian Y., Gatsogiannis C., Patasi C., Hofnagel O., Goody R. S., Farkasovský M., Raunser S.. 2013; The role of Cdc42 and Gic1 in the regulation of septin filament formation and dissociation. Elife2:e01085 [CrossRef][PubMed]
    [Google Scholar]
  61. Sinha I., Wang Y. M., Philp R., Li C. R., Yap W. H., Wang Y.. 2007; Cyclin-dependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev Cell13:421–432 [CrossRef][PubMed]
    [Google Scholar]
  62. Sirajuddin M., Farkasovsky M., Hauer F., Kühlmann D., Macara I. G., Weyand M., Stark H., Wittinghofer A.. 2007; Structural insight into filament formation by mammalian septins. Nature449:311–315 [CrossRef][PubMed]
    [Google Scholar]
  63. Takizawa P. A., DeRisi J. L., Wilhelm J. E., Vale R. D.. 2000; Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science290:341–344 [CrossRef][PubMed]
    [Google Scholar]
  64. Tang C. S., Reed S. I.. 2002; Phosphorylation of the septin cdc3 in g1 by the cdc28 kinase is essential for efficient septin ring disassembly. Cell Cycle1:42–29[PubMed]
    [Google Scholar]
  65. TerBush D. R., Maurice T., Roth D., Novick P.. 1996; The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae . EMBO J15:6483–6494[PubMed]
    [Google Scholar]
  66. Vargas-Muñiz J. M., Renshaw H., Richards A. D., Lamoth F., Soderblom E. J., Moseley M. A., Juvvadi P. R., Steinbach W. J.. 2015; The Aspergillus fumigatus septins play pleiotropic roles in septation, conidiation, and cell wall stress, but are dispensable for virulence. Fungal Genet Biol81:41–51 [CrossRef][PubMed]
    [Google Scholar]
  67. Vargas-Muñiz J. M., Renshaw H., Richards A. D., Waitt G., Soderblom E. J., Moseley M. A., Asfaw Y., Juvvadi P. R., Steinbach W. J.. 2016; Dephosphorylation of the core septin, AspB, in a protein phosphatase 2A-dependent manner impacts its localization and function in the fungal pathogen Aspergillus fumigatus . Front Microbiol7:997 [CrossRef][PubMed]
    [Google Scholar]
  68. Versele M., Thorner J.. 2004; Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J Cell Biol164:701–715 [CrossRef][PubMed]
    [Google Scholar]
  69. Warenda A. J., Konopka J. B.. 2002; Septin function in Candida albicans morphogenesis. Mol Biol Cell13:2732–2746 [CrossRef][PubMed]
    [Google Scholar]
  70. Warenda A. J., Kauffman S., Sherrill T. P., Becker J. M., Konopka J. B.. 2003; Candida albicans septin mutants are defective for invasive growth and virulence. Infect Immun71:4045–4051 [CrossRef][PubMed]
    [Google Scholar]
  71. Wightman R., Bates S., Amornrrattanapan P., Sudbery P.. 2004; In Candida albicans, the Nim1 kinases Gin4 and Hsl1 negatively regulate pseudohypha formation and Gin4 also controls septin organization. J Cell Biol164:581–591 [CrossRef][PubMed]
    [Google Scholar]
  72. Wolf W., Kilic A., Schrul B., Lorenz H., Schwappach B., Seedorf M.. 2012; Yeast Ist2 recruits the endoplasmic reticulum to the plasma membrane and creates a ribosome-free membrane microcompartment. PLoS One7:e39703 [CrossRef][PubMed]
    [Google Scholar]
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