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7 The Art of Networking: Vegetative Hyphal Fusion in Filamentous Ascomycete Fungi

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Part of the book series: The Mycota ((MYCOTA,volume 1))

Abstract

Hyphal fusion is a common feature of the growth and development of filamentous ascomycete fungi. It occurs at various developmental stages, most prominently during colony establishment by germinating spores and during the formation of cross connections within mature mycelial colonies. Recent years have seen great advances in understanding the biological roles and the molecular mechanisms of this fascinating biological process. It has become apparent that hyphal fusion promotes the formation of the mycelial network, thereby increasing fitness and competitiveness of the fungal colony. On the molecular level, an intricate signaling network controlling communication, attraction, and merger of fusing hyphae has been identified. This network comprises many well-conserved factors, including MAP kinases, reactive oxygen-generating systems, Ca2+-binding regulators, the STRIPAK complex, and cell polarity factors, which are partially adopted in novel and surprising ways. Studying the role and function of hyphal fusion therefore holds much potential to further our understanding not only of fungal growth and development but also of general eukaryotic cell biology.

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References

  • Aguilar PS, Baylies MK, Fleißner A, Helming L, Inoue N, Podbilewicz B, Wang H, Wong M (2013) Genetic basis of cell-cell fusion mechanisms. Trends Genet 29(7):427–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad SS, Miles PG (1970) Hyphal fusions in Schizophyllum commune. 2. Effects of environmental and chemical factors. Mycologia 62:1008–1017

    Google Scholar 

  • Aldabbous MS, Roca MG, Stout A, Huang IC, Read ND, Free SJ (2010) The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiology 156(Pt 9):2621–2629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartnicki-Garcia S, Bartnicki DD, Gierz G, Lopez-Franco R, Bracker CE (1995) Evidence that Spitzenkorper behavior determines the shape of a fungal hypha: a test of the hyphoid model. Exp Mycol 19(2):153–159

    CAS  PubMed  Google Scholar 

  • Baskarathevan J, Jaspers MV, Jones EE, Cruickshank RH, Ridgway HJ (2012) Genetic and pathogenic diversity of Neofusicoccum parvum in New Zealand vineyards. Fungal Biol 116(2):276–288

    CAS  PubMed  Google Scholar 

  • Bastiaans E, Debets AJ, Aanen DK (2015) Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition. Evolution 69:1091–1099

    PubMed  Google Scholar 

  • Becker Y, Eaton CJ, Brasell E, May KJ, Becker M, Hassing B, Cartwright GM, Reinhold L, Scott B (2015) The fungal cell-wall integrity MAPK cascade is crucial for hyphal network formation and maintenance of restrictive growth of Epichloe festucae in symbiosis with Lolium perenne. Mol Plant Microbe Interact 28(1):69–85

    PubMed  Google Scholar 

  • Bernhards Y, Poggeler S (2011) The phocein homologue SmMOB3 is essential for vegetative cell fusion and sexual development in the filamentous ascomycete Sordaria macrospora. Curr Genet 57:133–149

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bistis GN, Perkins DD, Read ND (2003) Different cell types in Neurospora crassa. Fungal Genet Newslett 50:17–19

    Google Scholar 

  • Blaise S, de Parseval N, Benit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100(22):13013–13018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bleichrodt RJ, van Veluw GJ, Recter B, Maruyama J, Kitamoto K, Wosten HA (2012) Hyphal heterogeneity in Aspergillus oryzae is the result of dynamic closure of septa by Woronin bodies. Mol Microbiol 86(6):1334–1344

    CAS  PubMed  Google Scholar 

  • Bloemendal S, Bernhards Y, Bartho K, Dettmann A, Voigt O, Teichert I, Seiler S, Wolters DA, Poggeler S, Kuck U (2012) A homologue of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol 84(2):310–323

    CAS  PubMed  Google Scholar 

  • Bodie EA, Armstrong GL, Dunn-Coleman NS (1994) Strain improvement of chymosin-producing strains of Aspergillus niger var. awamori using parasexual recombination. Enzyme Microb Technol 16(5):376–382

    CAS  PubMed  Google Scholar 

  • Buller A (1933) Researches on fungi, vol V. Longman, London

    Google Scholar 

  • Charlton ND, Shoji JY, Ghimire SR, Nakashima J, Craven KD (2012) Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte Epichloe festucae and the host plant. Eukaryot Cell 11(12):1463–1471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho W, Stahelin RV (2006) Membrane binding and subcellular targeting of C2 domains. Biochim Biophys Acta 1761(8):838–849

    CAS  PubMed  Google Scholar 

  • Choi KY, Satterberg B, Lyons DM, Elion EA (1994) Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78(3):499–512

    CAS  PubMed  Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160(Suppl 4):S99–S127

    PubMed  Google Scholar 

  • Collinge AJ, Markham P (1985) Woronin bodies rapidly plug septal pores of severed Penicillium chrysogenum hyphae. Exp Mycol 9:80–85

    Google Scholar 

  • Craven KD, Velez H, Cho Y, Lawrence CB, Mitchell TK (2008) Anastomosis is required for virulence of the fungal necrotroph Alternaria brassicicola. Eukaryot Cell 7(4):675–683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahlberg KR, Van Etten JL (1982) Physiology and biochemistry of fungal sporulation. Annu Rev Phytopathol 20:281–301

    CAS  Google Scholar 

  • De Bary A (1884) Vergleichende Morphologie und Biologie der Pilze, Mycetozoen und Bacterien. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Debets AJ, Swart K, Bos CJ (1990) Genetic analysis of Aspergillus niger: isolation of chlorate resistance mutants, their use in mitotic mapping and evidence for an eighth linkage group. Mol Gen Genet 221(3):453–458

    CAS  PubMed  Google Scholar 

  • Debets F, Swart K, Hoekstra RF, Bos CJ (1993) Genetic maps of eight linkage groups of Aspergillus niger based on mitotic mapping. Curr Genet 23(1):47–53

    CAS  PubMed  Google Scholar 

  • Dettmann A, Illgen J, März S, Schürg T, Fleißner A, Seiler S (2012) The NDR kinase scaffold HYM1/MO25 is essential for MAK2 MAP kinase signaling in Neurospora crassa. PLoS Genet 8(9), e1002950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dettmann A, Heilig Y, Ludwig S, Schmitt K, Illgen J, Fleißner A, Valerius O, Seiler S (2013) HAM-2 and HAM-3 are central for the assembly of the Neurospora STRIPAK complex at the nuclear envelope and regulate nuclear accumulation of the MAP kinase MAK-1 in a MAK-2-dependent manner. Mol Microbiol 90(4):796–812

    CAS  PubMed  Google Scholar 

  • Dettmann A, Heilig Y, Valerius O, Ludwig S, Seiler S (2014) Fungal communication requires the MAK-2 pathway elements STE-20 and RAS-2, the NRC-1 adapter STE-50 and the MAP kinase scaffold HAM-5. PLoS Genet 10(11), e1004762

    PubMed  PubMed Central  Google Scholar 

  • Dowson CG, Rayner ADM, Boddy L (1988) The form and outcome of mycelial interactions involving cord-forming decomposer basidiomycetes in homogeneous and heterogeneous environments. New Phytol 109:423–432

    Google Scholar 

  • Engh I, Wurtz C, Witzel-Schlomp K, Zhang HY, Hoff B, Nowrousian M, Rottensteiner H, Kuck U (2007) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot Cell 6(5):831–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer-Harman V, Jackson KJ, Munoz A, Shoji JY, Read ND (2012) Evidence for tryptophan being a signal molecule that inhibits conidial anastomosis tube fusion during colony initiation in Neurospora crassa. Fungal Genet Biol 49(11):896–902

    CAS  PubMed  Google Scholar 

  • Fleißner A (2012) Hyphal fusion. In: Perez-Martin J, Di Pietro A (eds) Morphogenesis and pathogenicity in fungi. Springer, Berlin, pp 43–60

    Google Scholar 

  • Fleißner A, Glass NL (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6(1):84–94

    PubMed  Google Scholar 

  • 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(5):920–930

    PubMed  PubMed Central  Google Scholar 

  • Fleißner A, Diamond S, Glass NL (2009a) The Saccharomyces cerevisiae PRM1 homolog in Neurospora crassa is involved in vegetative and sexual cell fusion events but also has postfertilization functions. Genetics 181(2):497–510

    PubMed  PubMed Central  Google Scholar 

  • Fleißner A, Leeder AC, Roca MG, Read ND, Glass NL (2009b) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci USA 106(46):19387–19392

    PubMed  PubMed Central  Google Scholar 

  • Frendo JL, Olivier D, Cheynet V, Blond JL, Bouton O, Vidaud M, Rabreau M, Evain-Brion D, Mallet F (2003) Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol Cell Biol 23(10):3566–3574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu C, Iyer P, Herkal A, Abdullah J, Stout A, Free SJ (2011) Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10(8):1100–1109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu C, Ao J, Dettmann A, Seiler S, Free SJ (2014) Characterization of the Neurospora crassa cell fusion proteins, HAM-6, HAM-7, HAM-8, HAM-9, HAM-10, AMPH-1 and WHI-2. PLoS ONE 9(10), e107773

    PubMed  PubMed Central  Google Scholar 

  • Giesbert S, Siegmund U, Schumacher J, Kokkelink L, Tudzynski P (2014) Functional analysis of BcBem1 and its interaction partners in Botrytis cinerea: impact on differentiation and virulence. PLoS ONE 9(5), e95172

    PubMed  PubMed Central  Google Scholar 

  • Glass NL, Dementhon K (2006) Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9(6):553–558

    CAS  PubMed  Google Scholar 

  • Glass NL, Kaneko I (2003) Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2(1):1–8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glass NL, Kuldau GA (1992) Mating type and vegetative incompatibility in filamentous ascomycetes. Annu Rev Phytopathol 30:201–224

    CAS  PubMed  Google Scholar 

  • Glass NL, Jacobson DJ, Shiu PK (2000) The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet 34:165–186

    CAS  PubMed  Google Scholar 

  • Goryachev AB, Lichius A, Wright GD, Read ND (2012) Excitable behavior can explain the “ping-pong” mode of communication between cells using the same chemoattractant. Bioessays 34:259–266

    CAS  PubMed  Google Scholar 

  • Harris MJ, Boddy L (2005) Nutrient movement and mycelial reorganization in established systems of Phanerochaete velutina, following arrival of colonized wood resources. Microb Ecol 50(2):141–151

    PubMed  Google Scholar 

  • Heiman MG, Walter P (2000) Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J Cell Biol 151(3):719–730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hickey PC, Jacobson D, Read ND, Louise Glass NL (2002) Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet Biol 37(1):109–119

    PubMed  Google Scholar 

  • Holmer L, Stenlid J (1993) The importance of inoculum size for the competitive ability of wood decomposing fungi. FEMS Microbiol Ecol 12:169–176

    Google Scholar 

  • Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67(7):2982–2992

    CAS  PubMed  PubMed Central  Google Scholar 

  • Howard RJ (1981) Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkorper, cytoskeleton and endomembranes after freeze-substitution. J Cell Sci 48:89–103

    CAS  PubMed  Google Scholar 

  • Huang G, Dougherty SD, Erdman SE (2009) Conserved WCPL and CX4C domains mediate several mating adhesin interactions in Saccharomyces cerevisiae. Genetics 182(1):173–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang HT, Maruyama J, Kitamoto K (2013) Aspergillus oryzae AoSO is a novel component of stress granules upon heat stress in filamentous fungi. PLoS ONE 8(8), e72209

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang J, Pallas DC (2014) STRIPAK complexes: structure, biological function, and involvement in human diseases. Int J Biochem Cell Biol 47:118–148

    CAS  PubMed  Google Scholar 

  • Hyakumachi M, Ui T (1987) Non-self-anastomosing isolates of Rhizoctonia solani obtained from fields of sugarbeet monoculture. Trans Br Mycol Soc 89(2):155–159

    Google Scholar 

  • Ishikawa FH, Souza EA, Read ND, Roca MG (2010) Live-cell imaging of conidial fusion in the bean pathogen, Colletotrichum lindemuthianum. Fungal Biol 114(1):2–9. doi:10.1016/j.funbio.2009.11.006, S1878-6146(09)00240-2 [pii]

    Article  PubMed  Google Scholar 

  • Ishikawa FH, Souza EA, Shoji JY, Connolly L, Freitag M, Read ND, Roca MG (2012) Heterokaryon incompatibility is suppressed following conidial anastomosis tube fusion in a fungal plant pathogen. PLoS ONE 7(2), e31175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs H, Boswell GP, Scrimgeour CM, Davidson FA, Gadd GM, Ritz K (2004) Translocation of carbon by Rhizoctonia solani in nutritionally-heterogeneous microcosms. Mycol Res 108(Pt 4):453–462

    PubMed  Google Scholar 

  • Jedd G (2007) Natural history of the fungal hypha: how Woronin bodies support a multicellular lifestyle. In: Gadd G, Watkinson SC, Dyer PS (eds) Fungi in the environment. Cambridge University Press, Cambridge, pp 22–37

    Google Scholar 

  • Jonkers W, Leeder AC, Ansong C, Wang Y, Yang F, Starr TL, Camp DG 2nd, Smith RD, Glass NL (2014) HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa. PLoS Genet 10(11), e1004783, PGENETICS-D-14-01795 [pii]

    PubMed  PubMed Central  Google Scholar 

  • Jun SC, Lee SJ, Park HJ, Kang JY, Leem YE, Yang TH, Chang MH, Kim JM, Jang SH, Kim HG, Han DM, Chae KS, Jahng KY (2011) The MpkB MAP kinase plays a role in post-karyogamy processes as well as in hyphal anastomosis during sexual development in Aspergillus nidulans. J Microbiol 49(3):418–430

    CAS  PubMed  Google Scholar 

  • Kasuga T, Glass NL (2008) Dissecting colony development of Neurospora crassa using mRNA profiling and comparative genomics approaches. Eukaryot Cell 7(9):1549–1564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Borkovich KA (2004) A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol Microbiol 52(6):1781–1798

    CAS  PubMed  Google Scholar 

  • Kim H, Borkovich KA (2006) Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot Cell 5(3):544–554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Köhler E (1929) Beiträge zur Kenntnis der vegetativen anastomosen der Pilze I. Planta 8:140–153

    Google Scholar 

  • Köhler E (1930) Zur Kenntnis der vegetativen Anastomosen der Pilze (II. Mitteilung). Planta 10:495–522

    Google Scholar 

  • Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ (2008) Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 18(22):1719–1726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laibach F (1928) Über Zellfusionen bei Pilzen. Planta 5:340–359

    Google Scholar 

  • Lamson RE, Takahashi S, Winters MJ, Pryciak PM (2006) Dual role for membrane localization in yeast MAP kinase cascade activation and its contribution to signaling fidelity. Curr Biol 16(6):618–623

    CAS  PubMed  Google Scholar 

  • Leeder AC, Palma-Guerrero J, Glass NL (2011) The social network: deciphering fungal language. Nat Rev Microbiol 9(6):440–451

    CAS  PubMed  Google Scholar 

  • Leeder AC, Jonkers W, Li J, Glass NL (2013) Early colony establishment in Neurospora crassa requires a MAP kinase regulatory network. Genetics 195(3):883–898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leeuw T, Fourest-Lieuvin A, Wu C, Chenevert J, Clark K, Whiteway M, Thomas DY, Leberer E (1995) Pheromone response in yeast: association of Bem1p with proteins of the MAP kinase cascade and actin. Science 270(5239):1210–1213

    CAS  PubMed  Google Scholar 

  • Leu LS (1967) Anastomosis in Venturia inaequalis (Cke.) Wint. PhD, University of Wisconsin, Madison

    Google Scholar 

  • Levin AM, de Vries RP, Conesa A, de Bekker C, Talon M, Menke HH, van Peij NN, Wosten HA (2007) Spatial differentiation in the vegetative mycelium of Aspergillus niger. Eukaryot Cell 6(12):2311–2322

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Wedlich-Soldner R (2009) Bem1 complexes and the complexity of yeast cell polarization. Curr Biol 19(5):R194–R195; author reply R195

    CAS  PubMed  Google Scholar 

  • Li D, Bobrowicz P, Wilkinson HH, Ebbole DJ (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170(3):1091–1104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lichius A, Lord KM (2014) Chemoattractive mechanisms in filamentous fungi. Open Mycol J 8(Suppl-1, M2):28–57

    Google Scholar 

  • Lichius A, Lord KM, Jeffree CE, Oborny R, Boonyarungsrit P, Read ND (2012) Importance of MAP kinases during protoperithecial morphogenesis in Neurospora crassa. PLoS ONE 7(8), e42565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lichius A, Goryachev AB, Fricker MD, Obara B, Castro-Longoria E, Read ND (2014) CDC-42 and RAC-1 regulate opposite chemotropisms in Neurospora crassa. J Cell Sci 127(Pt 9):1953–1965

    CAS  PubMed  Google Scholar 

  • Liu D, Novick P (2014) Bem1p contributes to secretory pathway polarization through a direct interaction with Exo70p. J Cell Biol 207(1):59–72

    PubMed  PubMed Central  Google Scholar 

  • Loera O, Cordova J (2003) Improvement of xylanase production by a parasexual cross between Aspergillus niger strains. Braz Arch Biol Technol 46(2):177–181

    CAS  Google Scholar 

  • Lopez-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A (2010) A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22(7):2459–2475

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maddi A, Dettman A, Fu C, Seiler S, Free SJ (2012) WSC-1 and HAM-7 are MAK-1 MAP kinase pathway sensors required for cell wall integrity and hyphal fusion in Neurospora crassa. PLoS ONE 7(8), e42374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maerz S, Ziv C, Vogt N, Helmstaedt K, Cohen N, Gorovits R, Yarden O, Seiler S (2008) The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179(3):1313–1325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Markham P (1994) Occlusions of septal pores in filamentous fungi. Mycol Res 98(10):1089–1106

    Google Scholar 

  • Maruyama J, Escano 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(1):868–873

    CAS  PubMed  Google Scholar 

  • Matheos D, Metodiev M, Muller E, Stone D, Rose MD (2004) Pheromone-induced polarization is dependent on the Fus3p MAPK acting through the formin Bni1p. J Cell Biol 165(1):99–109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mohler WA, Shemer G, del Campo JJ, Valansi C, Opoku-Serebuoh E, Scranton V, Assaf N, White JG, Podbilewicz B (2002) The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev Cell 2(3):355–362, doi:S1534580702001296 [pii]

    CAS  PubMed  Google Scholar 

  • Nordbring-Hertz B, Friman E, Veenhuis M (1989) Hyphal fusion during initial stages of trap formation in Arthrobotrys oligospora. Antonie Van Leeuwenhoek 55(3):237–244

    CAS  PubMed  Google Scholar 

  • Nordzieke S, Zobel T, Franzel B, Wolters DA, Kuck U, Teichert I (2014) A fungal SLMAP homolog plays a fundamental role in development and localizes to the nuclear envelope, ER, and mitochondria. Eukaryot Cell. doi:10.1128/EC.00241-14

    Article  PubMed  Google Scholar 

  • Palma-Guerrero J, Hall CR, Kowbel D, Welch J, Taylor JW, Brem RB, Glass NL (2013) Genome wide association identifies novel loci involved in fungal communication. PLoS Genet 9(8), e1003669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palma-Guerrero J, Leeder AC, Welch J, Glass NL (2014) Identification and characterization of LFD1, a novel protein involved in membrane merger during cell fusion in Neurospora crassa. Mol Microbiol 92(1):164–182

    CAS  PubMed  Google Scholar 

  • Pandey A, Roca MG, Read ND, Glass NL (2004) Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3(2):348–358

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22(2):153–183. doi:10.1210/edrv.22.2.0428

    Article  CAS  PubMed  Google Scholar 

  • Poggeler S, Kuck U (2004) A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3(1):232–240

    PubMed  PubMed Central  Google Scholar 

  • Pontecorvo G (1956) The parasexual cycle in fungi. Annu Rev Microbiol 10:393–400

    CAS  PubMed  Google Scholar 

  • Prados Rosales RC, Di Pietro A (2008) Vegetative hyphal fusion is not essential for plant infection by Fusarium oxysporum. Eukaryot Cell 7(1):162–171

    CAS  PubMed  Google Scholar 

  • Read ND, Fleißner A, Roca MG, Glass NL (2010) Hyphal fusion. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM Press, Washington, DC, pp 260–273

    Google Scholar 

  • Read ND, Goryachev AB, Lichius A (2012) The mechanistic basis of self-fusion between conidial anastomosis tubes during fungal colony initiation. Fungal Biol Rev 26:1–11

    Google Scholar 

  • Richard F, Glass NL, Pringle A (2012) Cooperation among germinating spores facilitates the growth of the fungus, Neurospora crassa. Biol Lett 8(3):419–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riquelme M, Reynaga-Pena CG, Gierz G, Bartnicki-Garcia S (1998) What determines growth direction in fungal hyphae? Fungal Genet Biol 24(1–2):101–109

    CAS  PubMed  Google Scholar 

  • Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E, Free SJ, Fleißner A, Freitag M, Lew RR, Mourino-Perez R, Plamann M, Rasmussen C, Richthammer C, Roberson RW, Sanchez-Leon E, Seiler S, Watters MK (2011) Architecture and development of the Neurospora crassa hypha -- a model cell for polarized growth. Fungal Biol 115(6):446–474

    PubMed  Google Scholar 

  • Roca MG, Davide LC, Mendes-Costa MC, Wheals A (2003) Conidial anastomosis tubes in Colletotrichum. Fungal Genet Biol 40(2):138–145

    PubMed  Google Scholar 

  • Roca MG, Davide LC, Davide LM, Mendes-Costa MC, Schwan RF, Wheals AE (2004) Conidial anastomosis fusion between Colletotrichum species. Mycol Res 108(Pt 11):1320–1326

    PubMed  Google Scholar 

  • Roca M, Read ND, Wheals AE (2005a) Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol Lett 249(2):191–198

    CAS  Google Scholar 

  • Roca MG, Arlt J, Jeffree CE, Read ND (2005b) Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4(5):911–919

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roca MG, Weichert M, Siegmund U, Tudzynski P, Fleißner A (2012) Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116(3):379–387

    CAS  PubMed  Google Scholar 

  • Roncal T, Cordobes S, Sterner O, Ugalde U (2002) Conidiation in Penicillium cyclopium is induced by conidiogenone, an endogenous diterpene. Eukaryot Cell 1(5):823–829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roper M, Ellison C, Taylor JW, Glass NL (2011) Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr Biol 21(18):R786–R793

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roper M, Simonin A, Hickey PC, Leeder A, Glass NL (2013) Nuclear dynamics in a fungal chimera. Proc Natl Acad Sci USA 110(32):12875–12880

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rothert W (1892) Über Sclerotium hydrophilum Sacc. einen sporenlosen Pilz. Botanische Zeitung 50:358–370

    Google Scholar 

  • Ruiz-Roldan MC, Kohli M, Roncero MI, Philippsen P, Di Pietro A, Espeso EA (2010) Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum. Eukaryot Cell 9(8):1216–1224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sapir A, Choi J, Leikina E, Avinoam O, Valansi C, Chernomordik LV, Newman AP, Podbilewicz B (2007) AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev Cell 12(5):683–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schurg T, Brandt U, Adis C, Fleißner A (2012) The Saccharomyces cerevisiae BEM1 homologue in Neurospora crassa promotes co-ordinated cell behaviour resulting in cell fusion. Mol Microbiol 86(2):349–366

    PubMed  Google Scholar 

  • Simon UK, Bauer R, Rioux D, Simard M, Oberwinkler F (2005) The vegetative life-cycle of the clover pathogen Cymadothea trifolii as revealed by transmission electron microscopy. Mycol Res 109(Pt 7):764–778

    PubMed  Google Scholar 

  • Simonin AR, Rasmussen CG, Yang M, Glass NL (2010) Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet Biol 47(10):855–868

    CAS  PubMed  Google Scholar 

  • Simonin A, Palma-Guerrero J, Fricker M, Glass NL (2012) Physiological significance of network organization in fungi. Eukaryot Cell 11(11):1345–1352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, Sumimoto H, Scott B (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc Natl Acad Sci USA 108(7):2861–2866

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teichert I, Steffens EK, Schnass N, Franzel B, Krisp C, Wolters DA, Kuck 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(9), e1004582

    PubMed  PubMed Central  Google Scholar 

  • Trinci APJ (1984) Regulation of hyphal branching and hyphal orientation. In: Jennings DH, Rayner ADM (eds) The ecology and physiology of the fungal mycelium. Cambridge University Press, Cambridge, UK, pp 23–52

    Google Scholar 

  • Trinci AP, Collinge AJ (1973) Structure and plugging of septa of wild type and spreading colonial mutants of Neurospora crassa. Arch Mikrobiol 91(4):355–364

    CAS  PubMed  Google Scholar 

  • Ward H (1888) A lily disease. Ann Bot 2(7):319–382

    Google Scholar 

  • Wei H, Requena N, Fischer R (2003) The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol Microbiol 47(6):1577–1588

    CAS  PubMed  Google Scholar 

  • Weichert M, Fleißner A (2015) Anastomosis and heterokaryon formation. In: Van den Berg M, Maruthachalam K (eds) Genetic transformation systems in fungi, vol 2. Springer, Heidelberg, pp 3–21

    Google Scholar 

  • Yokoyama K, Ogoshi A (1988) Studies on hyphal anastomosis of Rhizoctonia solani V. Nutritional conditions for anastomosis. Trans Mycol Soc Japan 29:125–132

    Google Scholar 

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Acknowledgment

Work in our group is supported by funding from the German Research Foundation (FL706-2) and the European Union (PITN-GA-2013-607963) to A.F.

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Correspondence to André Fleißner .

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Fleißner, A., Serrano, A. (2016). 7 The Art of Networking: Vegetative Hyphal Fusion in Filamentous Ascomycete Fungi. In: Wendland, J. (eds) Growth, Differentiation and Sexuality. The Mycota, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-25844-7_7

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