Abstract
In filamentous fungal species belonging to the Phyla Ascomycota and Basidiomycota, hyphae are compartmentalized into distinct cells by the formation of a septum. However, the septum does not completely separate hyphae due to the presence of a septal pore, which is a perforated structure that allows the exchange of the cytoplasmic constituents between adjacent hyphal cells. Cell-to-cell connectivity through the septal pore is associated with the catastrophic risk of cytoplasmic loss by cells adjacent to individually damaged hyphae. Pezizomycotina (filamentous Ascomycota) species have evolved to possess a specialized organelle called the Woronin body around the septum. The primary function of Woronin bodies is the prevention of excessive cytoplasmic loss from cells adjacent to damaged or lysed cells. Hex1, a major structural protein of Woronin bodies, is conserved in Pezizomycotina species. Woronin bodies differentiate from the peroxisomes and are typically tethered to the septum. Recent studies have identified additional septum-related components such as proteins containing intrinsically disordered regions and those involved in hyphal fusion/sexual reproduction and mitosis, which further elucidates molecular machineries governing the septal pore closure besides Woronin bodies.
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References
Asiegbu FO, Choi W, Jeong JS, Dean RA (2004) Cloning, sequencing and functional analysis of Magnaporthe grisea MVP1 gene, a hex-1 homolog encoding a putative “Woronin body” protein. FEMS Microbiol Lett 230:85–90
Beck J, Ebel F (2013) Characterization of the major Woronin body protein HexA of the human pathogenic mold Aspergillus fumigatus. Int J Med Microbiol 303:90–97
Beck J, Echtenacher B, Ebel F (2013) Woronin bodies, their impact on stress resistance and virulence of the pathogenic mould Aspergillus fumigatus and their anchoring at the septal pore of filamentous Ascomycota. Mol Microbiol 89:857–871
Berns MW, Aist JR, Wright WH, Liang H (1992) Optical trapping in animal and fungal cells using a tunable, near-infrared titanium-sapphire laser. Exp Cell Res 198:375–378
Bleichrodt RJ, van Veluw GJ, Recter B, Maruyama J, Kitamoto K, Wösten HA (2012) Hyphal heterogeneity in Aspergillus oryzae is the result of dynamic closure of septa by Woronin bodies. Mol Microbiol 86:1334–1344
Bleichrodt RJ, Hulsman M, Wösten HA, Reinders MJ (2015) Switching from a unicellular to multicellular organization in an Aspergillus niger hypha. MBio 6:e00111
Bowman JC, Scott Hicks P, Kurtz MB, Rosen H, Schmatz DM, Liberator PA, Douglas CM (2002) The antifungal echinocandin caspofungin acetate kills growing cells of Aspergillus fumigatus in vitro. Antimicrob Agents Chemother 46:3001–3012
Buller AHR (1933) The translocation of protoplasm through septate mycelium of certain Pyrenomycetes, Discomycetes and Hymenomycetes. In: Researches on fungi, vol 5. Longmans, Green & Co, London, pp 75–167
Camp RR (1977) Association of microbodies, Woronin bodies, and septa in intercellular hyphae of Cymadothea trifolii. Can J Bot 55:1856–1859
Curach NC, Te'o VS, Gibbs MD, Bergquist PL, Nevalainen KM (2004) Isolation, characterization and expression of the hex1 gene from Trichoderma reesei. Gene 331:133–140
Edgerton-Morgan H, Oakley BR (2012) gamma-Tubulin plays a key role in inactivating APC/C(Cdh1) at the G(1)-S boundary. J Cell Biol 198:785–791
Engh I, Würtz C, Witzel-Schlömp K, Zhang HY, Hoff B, Nowrousian M, Rottensteiner H, Kück U (2007) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot Cell 6:831–843
Escaño CS, Juvvadi PR, Jin FJ, Takahashi T, Koyama Y, Yamashita S, Maruyama J, Kitamoto K (2009) Disruption of the Aopex11-1 gene involved in peroxisome proliferation leads to impaired Woronin body formation in Aspergillus oryzae. Eukaryot Cell 8:296–305
Fiddy C, Trinci AP (1976) Mitosis, septation, branching and the duplication cycle in Aspergillus nidulans. J Gen Microbiol 97:169–184
Fleißner A, Glass NL (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6:84–94
Fleißner A, Sarkar S, Jacobson DJ, Roca MG, Read ND, Glass NL (2005) The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot Cell 4:920–930
Han P, Jin FJ, Maruyama J, Kitamoto K (2014) A large nonconserved region of the tethering protein Leashin is involved in regulating the position, movement, and function of Woronin bodies in Aspergillus oryzae. Eukaryot Cell 13:866–877
Jedd G (2011) Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol 21:12–19
Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226–231
Jedd G, Pieuchot L (2012) Multiple modes for gatekeeping at fungal cell-to-cell channels. Mol Microbiol 86:1291–1294
Juvvadi PR, Maruyama J, Kitamoto K (2007) Phosphorylation of the Aspergillus oryzae Woronin body protein, AoHex1, by protein kinase C: evidence for its role in the multimerization and proper localization of the Woronin body protein. Biochem J 405:533–540
Keller GA, Krisans S, Gould SJ, Sommer JM, Wang CC, Schliebs W, Kunau W, Brody S, Subramani S (1991) Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes. J Cell Biol 114:893–904
Kim KK, Hung LW, Yokota H, Kim R, Kim SH (1998) Crystal structures of eukaryotic translation initiation factor 5A from Methanococcus jannaschii at 1.8 A resolution. Proc Natl Acad Sci USA 95:10419–10424
Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl N, Cho Y, Mukhopadhyay B, Cramer RA Jr, Lawrence CB (2009) TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen. PLoS Pathog 5:e1000653
Kubo Y, Fujihara N, Harata K, Neumann U, Robin GP, O'Connell R (2015) Colletotrichum orbiculare FAM1 encodes a novel Woronin body-associated Pex22 peroxin required for appressorium-mediated plant infection. MBio 6:e01305–e01315
Lai J, Koh CH, Tjota M, Pieuchot L, Raman V, Chandrababu KB, Yang D, Wong L, Jedd G (2012) Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc Natl Acad Sci USA 109:15781–15786
Leonhardt Y, Kakoschke SC, Wagener J, Ebel F (2017) Lah is a transmembrane protein and requires Spa10 for stable positioning of Woronin bodies at the septal pore of Aspergillus fumigatus. Sci Rep 7:44179
Lew RR (2005) Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology 151:2685–2692
Li H, Oberhauser AF, Redick SD, Carrion-Vazquez M, Erickson HP, Fernandez JM (2001) Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc Natl Acad Sci USA 98:10682–10686
Li L, Wang J, Zhang Z, Wang Y, Liu M, Jiang H, Chai R, Mao X, Qiu H, Liu F, Sun G (2014) MoPex19, which is essential for maintenance of peroxisomal structure and Woronin bodies, is required for metabolism and development in the rice blast fungus. PLoS One 9:e85252
Lichius A, Yáñez-Gutiérrez ME, Read ND, Castro-Longoria E (2012) Comparative live-cell imaging analyses of SPA-2, BUD-6 and BNI-1 in Neurospora crassa reveal novel features of the filamentous fungal polarisome. PLoS One 7:e30372
Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180:325–339
Liu F, Lu Y, Pieuchot L, Dhavale T, Jedd G (2011) Import oligomers induce positive feedback to promote peroxisome differentiation and control organelle abundance. Dev Cell 21:457–468
Managadze D, Würtz C, Sichting M, Niehaus G, Veenhuis M, Rottensteiner H (2007) The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. Traffic 8:687–701
Markham P (1994) Occlusions of septal pores in filamentous fungi. Mycol Res 98:1089–1106
Markham P, Collinge AJ (1987) Woronin bodies of filamentous fungi. FEMS Microbiol Rev 46:1–11
Maruyama J, Kitamoto K (2007) Differential distribution of the endoplasmic reticulum network in filamentous fungi. FEMS Microbiol Lett 272:1–7
Maruyama J, Juvvadi PR, Ishi K, Kitamoto K (2005) Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 331:1081–1088
Maruyama J, Kikuchi S, Kitamoto K (2006) Differential distribution of the endoplasmic reticulum network as visualized by the BipA-EGFP fusion protein in hyphal compartments across the septum of the filamentous fungus, Aspergillus oryzae. Fungal Genet Biol 43:642–654
Maruyama J, Escaño CS, Kitamoto K (2010) AoSO protein accumulates at the septal pore in response to various stresses in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 391:868–873
Mason PJ, Crosse R (1975) Crystalline inclusions in hyphae of the glaucus group of Aspergilli. Trans Br Mycol Soc 65:129–134
McKeen WE (1971) Woronin bodies in Erysiphe graminis DC. Can J Microbiol 17:1557–1560
Momany M, Richardson EA, Van Sickle C, Jedd G (2002) Mapping Woronin body position in Aspergillus nidulans. Mycologia 94:260–266
Müller WH, Montijn RC, Humbel BM, van Aelst AC, Boon EJ, van der Krift TP, Boekhout T (1998) Structural differences between two types of basidiomycete septal pore caps. Microbiology 144:1721–1730
Nave R, Fürst DO, Weber K (1989) Visualization of the polarity of isolated titin molecules: a single globular head on a long thin rod as the M band anchoring domain? J Cell Biol 109:2177–2187
Nayak T, Edgerton-Morgan H, Horio T, Xiong Y, De Souza CP, Osmani SA, Oakley BR (2010) Gamma-tubulin regulates the anaphase-promoting complex/cyclosome during interphase. J Cell Biol 190:317–330
Ng SK, Liu F, Lai J, Low W, Jedd G (2009) A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning. PLoS Genet 5:e1000521
Oldfield CJ, Dunker AK (2014) Intrinsically disordered proteins and intrinsically disordered protein regions. Annu Rev Biochem 83:553–584
Peat TS, Newman J, Waldo GS, Berendzen J, Terwilliger TC (1998) Structure of translation initiation factor 5A from Pyrobaculum aerophilum at 1.75 A resolution. Structure 6:1207–1214
Plamann M (2009) Cytoplasmic streaming in Neurospora: disperse the plug to increase the flow? PLoS Genet 5:e1000526
Ryan FJ, Beadle GW, Tatum EL (1943) The tube method of measuring the growth rate of Neurospora. Am J Bot 30:784–799
Shen KF, Osmani AH, Govindaraghavan M, Osmani SA (2014) Mitotic regulation of fungal cell-to-cell connectivity through septal pores involves the NIMA kinase. Mol Biol Cell 25:763–775
Son M, Lee KM, Yu J, Kang M, Park JM, Kwon SJ, Kim KH (2013) The HEX1 gene of Fusarium graminearum is required for fungal asexual reproduction and pathogenesis and for efficient viral RNA accumulation of Fusarium graminearum virus 1. J Virol 87:10356–10367
Soundararajan S, Jedd G, Li X, Ramos-Pamploña M, Chua NH, Naqvi NI (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 6:1564–1574
Steinberg G, Schuster M, Hacker C, Kilaru S, Correia A (2017a) ATP prevents Woronin bodies from sealing septal pores in unwounded cells of the fungus Zymoseptoria tritici. Cell Microbiol 19:e12764
Steinberg G, Harmer NJ, Schuster M, Kilaru S (2017b) Woronin body-based sealing of septal pores. Fungal Genet Biol 109:53–55
Tegelaar M, Wösten HAB (2017) Functional distinction of hyphal compartments. Sci Rep 7:6039
Teichert I, Steffens EK, Schnaß N, Fränzel B, Krisp C, Wolters DA, Kück U (2014) PRO40 is a scaffold protein of the cell wall integrity pathway, linking the MAP kinase module to the upstream activator protein kinase C. PLoS Genet 10:e1004582
Tenney K, Hunt I, Sweigard J, Pounder JI, McClain C, Bowman EJ, Bowman BJ (2000) Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores. Fungal Genet Biol 31:205–217
Tey WK, North AJ, Reyes JL, Lu YF, Jedd G (2005) Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol Biol Cell 16:2651–2659
Trinci APJ, Collinge AJ (1974) Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals. Protoplasma 80:57–67
Wergin WP (1973) Development of Woronin bodies from microbodies in Fusarium oxysporum f. sp. lycopersici. Protoplasma 76:249–260
Woronin M (1864) Zur Entwicklungsgeschichte der Ascobolus pulcherrimus Cr und eigiger Pezizen. Abh Senkenb Naturforsch Ges 5:333–344
Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19:31–38
Würtz C, Schliebs W, Erdmann R, Rottensteiner H (2008) Dynamin-like protein-dependent formation of Woronin bodies in Saccharomyces cerevisiae upon heterologous expression of a single protein. FEBS J 275:2932–2941
Yuan P, Jedd G, Kumaran D, Swaminathan S, Shio H, Hewitt D, Chua NH, Swaminathan K (2003) A HEX-1 crystal lattice required for Woronin body function in Neurospora crassa. Nat Struct Biol (4):264–270
Zekert N, Veith D, Fischer R (2010) Interaction of the Aspergillus nidulans microtubule-organizing center (MTOC) component ApsB with gamma-tubulin and evidence for a role of a subclass of peroxisomes in the formation of septal MTOCs. Eukaryot Cell 9:795–805
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Maruyama, Ji., Kitamoto, K. (2019). The Woronin Body: A Fungal Organelle Regulating Multicellularity. In: Hoffmeister, D., Gressler, M. (eds) Biology of the Fungal Cell. The Mycota, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-05448-9_1
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