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Hyphal Fusion

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Morphogenesis and Pathogenicity in Fungi

Part of the book series: Topics in Current Genetics ((TCG,volume 22))

Abstract

Since the early days of mycology, hyphal fusion or anastomosis has been recognized as a common feature of colony establishment and development in filamentous fungi. However, the role and function of this process remained mostly unclear. In recent years, much progress in understanding the molecular basis of anastomosis has been made, and numerous genes and proteins essential for fusion were identified. Insights emerging from these studies include the notion that hyphal fusion employs conserved signaling pathways, but adopts them in unusually dynamic fashions. In addition, increasing evidence suggests that anastomosis formation and pathogenic hyphal development share common machineries to some extent. Future challenges in studying hyphal fusion include deciphering the molecular networks controlling this complex cellular process and understanding the biological function of anastomosis.

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References

  • 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 156:2621–2629

    Article  PubMed  CAS  Google Scholar 

  • Beckett A, Wilson IM (1968) Ascus cytology of Podospora anserina. J Gen Microbiol 53:81–87

    PubMed  CAS  Google Scholar 

  • Begueret J, Turcq B, Clave C (1994) Vegetative incompatibility in filamentous fungi: het genes begin to talk. Trends Genet 10:441–446

    Article  PubMed  CAS  Google Scholar 

  • Benoist M, Gaillard S, Castets F (2006) The striatin family: a new signaling platform in dendritic spines. J Physiol Paris 99:146–153

    Article  PubMed  CAS  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(2):133–149

    Article  PubMed  CAS  Google Scholar 

  • Bistis GN (1981) Chemotropic interactions between trichogynes and conidia of opposite mating-type in Neurospora crassa. Mycologia 73:959–975

    Article  Google Scholar 

  • Bistis GN (1996) Trichogynes and fertilization in uni- and bimating type colonies of Neurospora tetrasperma. Fungal Genet Biol 20:93–98

    Article  PubMed  Google Scholar 

  • Bloemendal S, Lord KM, Rech C, Hoff B, Engh I, Read ND, Kuck U (2010) A mutant defective in sexual development produces aseptate ascogonia. Eukaryot Cell 9:1856–1866

    Article  PubMed  CAS  Google Scholar 

  • Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ (2002) The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol Microbiol 45:795–804

    Article  PubMed  CAS  Google Scholar 

  • Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER, O’Rourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108

    Article  PubMed  CAS  Google Scholar 

  • Bos CJ, Debets AJ, Huybers A, Kobus G, Slakhorst SM (1988) Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger. Curr Genet 14:437–443

    Article  PubMed  CAS  Google Scholar 

  • Bowman SM, Piwowar A, Al Dabbous M, Vierula J, Free SJ (2006) Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryot Cell 5:587–600

    Article  PubMed  CAS  Google Scholar 

  • Bowman SM, Piwowar A, Arnone ED, Matsumoto R, Koudelka GB, Free SJ (2009) Characterization of GPIT-1 and GPIT-2, two auxiliary components of the Neurospora crassa GPI transamidase complex. Mycologia 101:764–772

    Article  PubMed  CAS  Google Scholar 

  • Bruggeman J, Debets AJ, Swart K, Hoekstra RF (2003) Male and female roles in crosses of Aspergillus nidulans as revealed by vegetatively incompatible parents. Fungal Genet Biol 39:136–141

    Article  PubMed  CAS  Google Scholar 

  • Buller A (1931) Researches on fungi. Longman, London

    Google Scholar 

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

    Google Scholar 

  • Caddick MX, Peters D, Platt A (1994) Nitrogen regulation in fungi. Antonie Van Leeuwenhoek 65:169–177

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Wu H (1977) Hyphal anastomosis in Pyricularia oryzae. Protoplasma 92:281–287

    Article  Google Scholar 

  • Collinge AJ, Markham P (1987) Woronin bodies rapidly plug septal pores of severed Penicillium chrysogenum hyphae. Exp Mycol 9:80–85

    Article  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 7:675–683

    Article  PubMed  CAS  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

    Article  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 6:831–843

    Article  PubMed  CAS  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 4:920–930

    Article  PubMed  CAS  Google Scholar 

  • Fleissner A, Simonin AR, Glass NL (2008) Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol Biol 475:21–38

    Article  PubMed  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 181:497–510

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gierz G, Bartnicki-Garcia S (2001) A three-dimensional model of fungal morphogenesis based on the vesicle supply center concept. J Theor Biol 208:151–164

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Glass NL, Rasmussen C, Roca MG, Read ND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12:135–141

    Article  PubMed  CAS  Google Scholar 

  • Guzzo RM, Wigle J, Salih M, Moore ED, Tuana BS (2004) Regulated expression and temporal induction of the tail-anchored sarcolemmal-membrane-associated protein is critical for myoblast fusion. Biochem J 381:599–608

    Article  PubMed  CAS  Google Scholar 

  • Hay FS (1995) Unusual germination of spores of Arthrobotrys conoides and A. cladodes. Mycol Res 99:981–982

    Article  Google Scholar 

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

    Article  PubMed  CAS  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 37:109–119

    Article  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

    Article  Google Scholar 

  • Hou Z, Katan T, Kistler HC, Xu JR (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15:1119–1127

    Article  PubMed  CAS  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 114:2–9

    Article  PubMed  Google Scholar 

  • Jeffries P (1985) Mycoparasitism within the zygomycetes. Bot J Linnean Soc 91:135–150

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kays AM, Borkovich KA (2004) Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics 166:1229–1240

    Article  PubMed  CAS  Google Scholar 

  • Kellner M, Burmester A, Wostemeyer A, Wostemeyer J (1993) Transfer of genetic information from the mycoparasite Parasitella parasitica to its host Absidia glauca. Curr Genet 23:334–337

    Article  PubMed  CAS  Google Scholar 

  • Kemp HA, Sprague GF Jr (2003) Far3 and five interacting proteins prevent premature recovery from pheromone arrest in the budding yeast Saccharomyces cerevisiae. Mol Cell Biol 23:1750–1763

    Article  PubMed  CAS  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 52:1781–1798

    Article  PubMed  CAS  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 5:544–554

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Metzenberg RL, Nelson MA (2002) Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Eukaryot Cell 1:987–999

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Krystofova S, Borkovich KA (2005) The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gbetagamma dimer required for normal female fertility, asexual development, and galpha protein levels in Neurospora crassa. Eukaryot Cell 4:365–378

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Latunde-Dada A, O’Conell R, Nash C, Lucas J (1999) Stomatal penetration of cowpea (Vigna unguiculata) leaves by a Colletotrichum species causing latent anthracnose. Plant Pathology 48:777–785

    Article  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 22:2459–2475

    Article  PubMed  CAS  Google Scholar 

  • Loubradou G, Turcq B (2000) Vegetative incompatibility in filamentous fungi: a roundabout way of understanding the phenomenon. Res Microbiol 151:239–245

    Article  PubMed  CAS  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 179:1313–1325

    Article  PubMed  CAS  Google Scholar 

  • Maerz S, Dettmann A, Ziv C, Liu Y, Valerius O, Yarden O, Seiler S (2009) Two NDR kinase-MOB complexes function as distinct modules during septum formation and tip extension in Neurospora crassa. Mol Microbiol 74:707–723

    Article  PubMed  CAS  Google Scholar 

  • Markham P, Collinge AJ (1987) Woronin bodies of filamentous fungi. FEMS Microbiol Rev 46:1–11

    Article  Google Scholar 

  • Martin DE, Hall MN (2005) The expanding TOR signaling network. Curr Opin Cell Biol 17:158–166

    Article  PubMed  CAS  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

    Google Scholar 

  • McCabe P, Gallagher M, Deacon J (1999) Microscopic observation of perfect hyphal fusion in Rhizoctonia solani. Mycol Res 103

    Google Scholar 

  • Naito H (1978) Hyphal fusion in Fusarium leaf spot fungus of rice plants. Trans Mycol Soc Japan 19:11–21

    Google Scholar 

  • Newhouse J, MacDonald W (1991) The ultrastructure of hyphal anastomoses between vegetatively compatible and incompatible virulent and hypovirulent strains of Cryphonectria parasitica. Can J Bot 69:602–614

    Article  Google Scholar 

  • Oren-Suissa M, Podbilewicz B (2010) Evolution of programmed cell fusion: common mechanisms and distinct functions. Dev Dyn 239:1515–1528

    Article  PubMed  CAS  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 3:348–358

    Article  PubMed  CAS  Google Scholar 

  • Poggeler S, Kuck U (2001) Identification of transcriptionally expressed pheromone receptor genes in filamentous ascomycetes. Gene 280:9–17

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Raju NB (1980) Meiosis and ascospore genesis in Neurospora. Eur J Cell Biol 23:208–223

    PubMed  CAS  Google Scholar 

  • Read ND, Roca MG (2006) Vegetative hyphal fusion in filamentous fungi. In: Baluska F, Volkmann D, Barlow PW (eds) Cell–Cell channels. Landes Bioscience, Georgetown, TX, pp 87–98

    Chapter  Google Scholar 

  • Read ND, Lichius A, Shoji JY, Goryachev AB (2009) Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12:608–615

    Article  PubMed  Google Scholar 

  • Rech C, Engh I, Kuck U (2007) Detection of hyphal fusion in filamentous fungi using differently fluorescence-labeled histones. Curr Genet 52:259–266

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Riquelme M, Bartnicki-Garcia S, Gonzalez-Prieto JM, Sanchez-Leon E, Verdin-Ramos JA, Beltran-Aguilar A, Freitag M (2007) Spitzenkorper localization and intracellular traffic of green fluorescent protein-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot Cell 6:1853–1864

    Article  PubMed  CAS  Google Scholar 

  • Rispail N, Di Pietro A (2009) Fusarium oxysporum Ste12 controls invasive growth and virulence downstream of the Fmk1 MAPK cascade. Mol Plant Microbe Interact 22:830–839

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 108:1320–1326

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roca MG, Kuo HC, Lichius A, Freitag M, Read ND (2010) Nuclear dynamics, mitosis, and the cytoskeleton during the early stages of colony initiation in Neurospora crassa. Eukaryot Cell 9:1171–1183

    Article  PubMed  CAS  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 9:1216–1224

    Article  PubMed  CAS  Google Scholar 

  • Satina S, Blakeslee AF (1926) The Mucor parasite Parasitella in relation to sex. Proc Natl Acad Sci USA 12:202–207

    Article  PubMed  CAS  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 47:855–868

    Article  PubMed  CAS  Google Scholar 

  • Soulard A, Cohen A, Hall MN (2009) TOR signaling in invertebrates. Curr Opin Cell Biol 21:825–836

    Article  PubMed  CAS  Google Scholar 

  • Swart K, Debets AJ, Bos CJ, Slakhorst M, Holub EF, Hoekstra RF (2001) Genetic analysis in the asexual fungus Aspergillus niger. Acta Biol Hung 52:335–343

    Article  PubMed  CAS  Google Scholar 

  • Szewczyk E, Krappmann S (2010) Conserved regulators of mating are essential for Aspergillus fumigatus cleistothecium formation. Eukaryot Cell 9:774–783

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Trinci APJ (1984) Regualtion 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 

  • van Drogen F, Stucke VM, Jorritsma G, Peter M (2001) MAP kinase dynamics in response to pheromones in budding yeast. Nat Cell Biol 3:1051–1059

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Wong KH, Hynes MJ, Todd RB, Davis MA (2007) Transcriptional control of nmrA by the bZIP transcription factor MeaB reveals a new level of nitrogen regulation in Aspergillus nidulans. Mol Microbiol 66:534–551

    Article  PubMed  CAS  Google Scholar 

  • Woronin M (1864) Zur Entwicklungsgeschichte der Ascobolus pulcherrimus Cr. und einiger Pezizen. Abh Senkenb Naturforsch 5:333–344

    Google Scholar 

  • Xiang Q, Rasmussen C, Glass NL (2002) The ham-2 locus, encoding a putative transmembrane protein, is required for hyphal fusion in Neurospora crassa. Genetics 160:169–180

    PubMed  CAS  Google Scholar 

  • Zhao X, Mehrabi R, Xu JR (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6:1701–1714

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

I thank Dr. Carolyn Rasmussen and Timo Schürg for critical reading of the manuscript.

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Correspondence to André Fleißner .

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Fleißner, A. (2012). Hyphal Fusion. In: Pérez-Martín, J., Di Pietro, A. (eds) Morphogenesis and Pathogenicity in Fungi. Topics in Current Genetics, vol 22. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22916-9_3

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