Skip to main content

15 Fruiting Body Formation in Basidiomycetes

  • Chapter
  • First Online:

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

Abstract

Establishment of the dikaryotic mycelium and formation of fruiting bodies are highly complex developmental programmes that are activated by a combination of environmental cues. A wide variety of proteins are expected to regulate and coordinate these programmes or to fulfil enzymatic conversions or structural roles. With the identification of the first genes involved in mushroom development, we are only at the beginning of understanding fruiting body formation. The process of identification of genes will be accelerated by whole genome expression studies and increased availability of molecular tools to assign functions to genes.

Establishment of the dikaryon and emergence of fruiting bodies in basidiomycetes are regulated by the mating-type genes. These genes encode DNA-binding proteins and pheromones and their receptors. Regulation of fruiting by the mating-type genes is mediated by downstream transcription factors. Several genes encoding such regulatory proteins have now been identified. Regulatory circuits ultimately activate genes encoding structural proteins or enzymes that are involved in fruiting body formation. The role of hydrophobins is well established. They enable hyphae to escape the aqueous environment to allow fruiting body development. Moreover, they coat aerial structures and line air channels in mushrooms. The hydrophobic coating irreversibly directs growth of hyphae into the air, allows dispersal of spores and ensures gas exchange in fruiting bodies under humid conditions. Apart from hydrophobins, phenolics polymerised by the action of laccases may contribute to surface hydrophobicity of fruiting bodies. These enzymes have also been proposed to cross-link cell walls of hyphae in the fruiting bodies but this still has to be established. Experimental evidence indicates that cytochrome P450 enzymes, lectins, haemolysins and expansins also function in mushroom development. Lectins may be involved in aggregation of hyphae, haemolysins in signalling particularly to induce apoptosis of selected hyphae in the fruiting body, while expansins may be involved in cell wall modification and extension.

This is a preview of subscription content, log in via an institution.

References

  • Ásgeirsdóttir SA, van Wetter MA, Wessels JGH (1995) Differential expression of genes under control of the mating-type genes in the secondary mycelium of Schizophyllum commune. Microbiology 141:1281–1288

    PubMed  Google Scholar 

  • Ásgeirsdóttir SA, Halsall JR, Casselton LA (1997) Expression of two closely linked hydrophobin genes of Coprinus cinereus is monokaryon-specific and down-regulated by the oid-1 mutation. Fungal Genet Biol 22:54–63

    PubMed  Google Scholar 

  • Ásgeirsdóttir SA, de Vries OMH, Wessels JGH (1998) Identification of three differentially expressed hydrophobins in Pleurotus ostreatus (oyster mushroom). Microbiology 144:2961–2969

    Google Scholar 

  • Bahn YS, Muhlschlegel FA (2006) CO2 sensing in fungi and beyond. Curr Opin Microbiol 9:572–578

    CAS  PubMed  Google Scholar 

  • Bakkeren G, Kronstad JW (1994) Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci USA 91:7085–7089

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bayram Ö, Biesemann C, Krappmann S, Galland P, Braus GH (2008a) More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol Biol Cell 19:3254–3262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH (2008b) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506

    CAS  PubMed  Google Scholar 

  • Bayram Ö, Braus GH, Fischer R, Rodriguez-Romero J (2010) Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet Biol 47:900–908

    CAS  PubMed  Google Scholar 

  • Berne S, Križaj I, Pohleven F, Turk T, Maček P, Sepčić K (2002) Pleurotus and Agrocybe hemolysins, new proteins hypothetically involved in fungal fruiting. Biochem Biophys Acta 1570:153–159

    CAS  PubMed  Google Scholar 

  • Berne S, Pohleven J, Vidic I, Rebolj K, Pohleven F, Turk T, Maček P, Sonnenberg A, Sepčić K (2007) Ostreolysin enhances fruiting initiation in the oyster mushroom (Pleurotus ostreatus). Mycol Res 111(12):1431–1436

    CAS  PubMed  Google Scholar 

  • Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fischer R (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15:1833–1838

    CAS  PubMed  Google Scholar 

  • Boulianne RP, Liu Y, Aebi M, Lu BC, Kües U (2000) Fruiting body development in Coprinus cinereus: regulated expression of two galectins secreted by a non classical pathway. Microbiology 146:1841–1853

    CAS  PubMed  Google Scholar 

  • Bouzeralou D, Billini M, Roumelioti K, Sophianopoulou V (2008) EglD, a putative endoglucanase, with an expansin like domain is localized in the conidial cell wall of Aspergillus nidulans. Fungal Genet Biol 45:839–850

    Google Scholar 

  • Bu’Lock JD (1967) Essays in biosynthesis and microbial development. In: Squibb ER (ed) Essays in biosynthesis and microbial development, lectures on chemistry and microbial products. Wiley, New York, pp 1–18

    Google Scholar 

  • Bu’Lock JD, Walker DC (1967) On chagi. J Chem Soc Sect C 5:336–338

    Google Scholar 

  • Butko P, Buford JP, Goodwin JS, Stroud PA, McCormick CL, Cannon GC (2001) Spectroscopic evidence for amyloid-like interfacial self-assembly of hydrophobin Sc3. Biochem Biophys Res Commun 280:212–215

    CAS  PubMed  Google Scholar 

  • Chiu S-W, Moore D (eds) (1996) Patterns in fungal development. Cambridge University Press, Cambridge

    Google Scholar 

  • Clémonçon H (1997) Anatomy of the hymenomycetes. An introduction to the cytology and plectology of crust fungi, bracket fungi, club fungi, Chantarelles, Agarics and Boletes. F. Flück-Wirth, Teufen, Switzerland

    Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850–861

    CAS  PubMed  Google Scholar 

  • de Groot PWJ, Schaap PJ, Sonnenberg ASM, Visser J, Van Griensven LJLD (1996) The Agaricus bisporus hypA gene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J Mol Biol 257:1008–1018

    PubMed  Google Scholar 

  • de Groot PWJ, Roeven RT, Van Griensven LJ, Visser J, Schaap PJ (1999) Different temporal and spatial expression of two hydrophobin-encoding genes of the edible mushroom Agaricus bisporus. Microbiology 145:1105–1113

    PubMed  Google Scholar 

  • de Vocht ML, Scholtmeijer K, van der Vegte EW, de Vries OMH, Sonveaux N, Wösten HAB, Ruysschaert J-M, Hadziioannou G, Wessels JGH, Robillard GT (1998) Structural characterization of the hydrophobin SC3, as a monomer and after self-assembly at hydrophobic/hydrophilic interfaces. Biophys J 74:2059–2068

    PubMed  PubMed Central  Google Scholar 

  • de Vocht ML, Reviakine I, Ulrich WP, Bergsma‐Schutter W, Wösten HAB, Vogel H, Brisson A, Wessels JGH, Robillard GT (2002) Self‐assembly of the hydrophobin SC3 proceeds via two structural intermediates. Protein Sci 11:1199–1205

    PubMed  PubMed Central  Google Scholar 

  • Durand R (1985) Blue U.V.-light photoreception in fungi. Rev Physiol Végét 23:935–943

    Google Scholar 

  • Dyer PS, Inderbitzin P, Debuchy R (2016) Mating-type structure, function, regulation and evolution in the pezizomycotina. In: Wendland J (ed) Growth, differentiation and sexuality. Springer, Cham, pp 351–385

    Google Scholar 

  • Eastwood DC, Herman B, Noble R, Dobrovin-Pennington A, Sreenivasaprasad S, Burton KS (2013) Environmental regulation of reproductive phase change in Agaricus bisporus by 1-octen-3-ol, temperature and CO2. Fungal Genet Biol 55:54–66

    CAS  PubMed  Google Scholar 

  • Erdmann S, Freihorst D, Raudaskoski M, Schmidt-Heck W, Jung EM, Senftleben D, Kothe E (2012) Transcriptome and functional analysis of mating in the basidiomycete Schizophyllum commune. Eukaryot Cell 11:571–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang H, Zhang W, Niu X, Liu Z, Lu C, Wei H, Yuan S (2014) Stipe wall extension of Flammulina velutipes could be induced by an expansin-like protein from Helix aspersa. Fungal Biol 118(1):1–11

    CAS  PubMed  Google Scholar 

  • Faumann EB, Blumenthal RM, Cheng XD (1999) Structure and evolution of AdoMet-dependent methyltransferases. In: Cheng XD, Blumenthal RM (eds) S-adenosylmethionine-dependent methyltransferases: structures and functions. World Scientific, Singapore, pp 1–38

    Google Scholar 

  • Fernandez Espinar MT, Labarère J (1997) Cloning and sequencing of the Aa-pri1 gene specifically expressed during fruiting initiation in the edible mushroom Agrocybe aegerita. Curr Genet 32:420–424

    CAS  PubMed  Google Scholar 

  • Fowler TJ, Mitton MF (2000) Scooter, a new active transposon in Schizophyllum commune, has disrupted two genes regulating signal transduction. Genetics 156:1585–1594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freihorst D, Fowler TJ, Bartholomew K, Marjatta R, Stephen Horton J, Kothe E (2016) The mating type genes of the basidiomycetes. In: Wendland J (ed) Growth, differentiation and sexuality. Springer, Cham, pp 329–349

    Google Scholar 

  • Grillo R, Korhonen K, Hantula J, Hietala AM (2000) Genetic evidence of somatic haploidization in developing fruit bodies of Armillaria tabescens. Fungal Genet Biol 30:135–145

    CAS  PubMed  Google Scholar 

  • Han C-H, Zhang G-Q, Wang H-X, Ng TB (2010) Schizolysin, a hemolysin from the split gill mushroom Schizophyllum commune. FEMS Microbiol Lett 309(2):115–121

    CAS  PubMed  Google Scholar 

  • Horton JS, Raper CA (1991) A mushroom-inducing DNA sequence isolated from the basidiomycete Schizophyllum commune. Genetics 129:707–716

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horton JS, Raper CA (1995) The mushroom-inducing gene FRT1 of Schizophyllum commune encodes a putative nucleotide binding protein. Mol Gen Genet 247:358–366

    CAS  PubMed  Google Scholar 

  • Horton JS, Palmer GE, Smith WJ (1999) Regulation of dikaryon-expressed genes by FRT1 in the basidiomycete Schizophyllum commune. Fungal Genet Biol 26:33–47

    CAS  PubMed  Google Scholar 

  • Inada K, Morimoto Y, Arima T, Murata Y, Kamada T (2001) The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics 157:133–140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa H (1967) Physiological and ecological studies on Lentinus edodes (Berk.) Sing. J Agric Lab 8:1–57

    Google Scholar 

  • James TY, Srivilai P, Kües U, Vilgalys R (2006) Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics 172(3):1877–1891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jennings DH (1984) Water flow through mycelia. In: Jennings DH, Rayner ADM (eds) The ecology and physiology of fungal mycelia. Cambridge University Press, Cambridge, pp 143–164

    Google Scholar 

  • Kamada T (2002) Molecular genetics of sexual development in the mushroom Coprinus cinereus. BioEssays 24:449–459

    CAS  PubMed  Google Scholar 

  • Kamada T, Kurita R, Takemaru T (1978) Effects of light on basidiocarp maturation in Coprinus macrorhizus. Plant Cell Physiol 19:263–275

    Google Scholar 

  • Kamada T, Sano H, Nakazawa T, Nakahori K (2010) Regulation of fruiting body photomorphogenesis in Coprinopsis cinerea. Fungal Genet Biol 47:917–921

    PubMed  Google Scholar 

  • Kershaw MJ, Wakley G, Talbot NJ (1998) Complementation of the mpg1 mutant phenotype in Magnaporthe grisea reveals functional relationships between fungal hydrophobins. EMBO J 17:3838–3849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kertesz-Chaloupková K, Walser PJ, Granado JD, Aebi M, Kües U (1998) Blue light overrides repression of a-sexual sporulation by mating type genes in the basidiomycete Coprinus cinereus. Fungal Genet Biol 23:95–109

    PubMed  Google Scholar 

  • Kim H, Han K, Kim K, Han D, Jahng K, Chae K (2002) The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet Biol 37:72–80

    CAS  PubMed  Google Scholar 

  • Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schröppel K, Naglik JR, Eckert SE, Mogensen EG, Haynes K, Tuite MF, Levin LR, Buck J, Mühlschlegel FA (2005) Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15:2021–2026

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knabe N, Jung E-M, Freihorst D, Hennicke F, Horton JS, Kothe E (2013) A central role for Ras1 in morphogenesis of the basidiomycete Schizophyllum commune. Eukaryot Cell 12(6):941–952

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koltin Y (1970) Development of the AmutBmut strain of Schizophyllum commune. Arch Microbiol 74:123–128

    Google Scholar 

  • Kothe E (2001) Mating-type genes for basidiomycete strain improvement in mushroom farming. Appl Microbiol Biotechnol 56:602–612

    CAS  PubMed  Google Scholar 

  • Kües U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353

    PubMed  PubMed Central  Google Scholar 

  • Kües U, Liu Y (2000) Fruiting body production in basidiomycetes. Appl Microbiol Biotechnol 54:141–152

    PubMed  Google Scholar 

  • Kües U, Künzler M, Bottoli APF, Walser PJ, Granado JD, Yi L, Bertossa RC, Ciardo D, Clergeot P-H, Loos S, Ruprich-Robert G, Aebi M (2004) Mushroom development in higher basidiomycetes; implications for human and animal health. In: Kushwaha RKS (ed) Fungi in human and animal health. Scientific, Jodhpur, India, pp 431–469

    Google Scholar 

  • Kües U, Badalyan SM, Gießler A, Dörnte B (2016) Asexual sporulation in agaricomycetes. In: Wendland J (ed) Growth, differentiation and sexuality. Springer, Cham, pp 269–328

    Google Scholar 

  • Kuratani M, Tanaka K, Terashima K, Muraguchi H, Nakazawa T, Nakahori K, Kamada T (2010) The dst2 gene essential for photomorphogenesis of Coprinopsis cinerea encodes a protein with a putative FAD-binding-4 domain. Fungal Genet Biol 47:152–158

    CAS  PubMed  Google Scholar 

  • Lee BN, Adams TH (1994) Overexpression of flbA, an early regulator of Aspergillus asexual sporulation, leads to activation of brlA and premature initiation of development. Mol Microbiol 14:323–334

    CAS  PubMed  Google Scholar 

  • Lengerer KB, Fox DS, Fraser JA, Allen A, Forrester K, Dietrich FS, Heitman J (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell 1(5):704–718

    Google Scholar 

  • Lu BC (1974) Meiosis in Coprinus. Role of light on basidiocarp initiation, mitosis, and hymenium differentiation in Coprinus lagopus. Can J Bot 52:299–308

    Google Scholar 

  • Lu BC (2000) The control of meiosis progression in the fungus Coprinus cinereus by light/dark cycles. Fungal Genet Biol 31:33–41

    CAS  PubMed  Google Scholar 

  • Luan R, Liang Y, Chen Y, Liu H, Jiang S, Che T, Wong B, Sun Hui H (2010) Opposing developmental functions of Agrocybe aegerita galectin (AAL) during mycelia differentiation. Fungal Biol 114(8):599–608

    CAS  PubMed  Google Scholar 

  • Lugones LG, Bosscher JS, Scholtmeijer K, de Vries OMH, Wessels JGH (1996) An abundant hydrophobin (ABH1) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142:1321–1329

    CAS  PubMed  Google Scholar 

  • Lugones LG, Wösten HAB, Wessels JGH (1998) A hydrophobin (ABH3) secreted by the substrate mycelium of Agaricus bisporus (common white button mushroom). Microbiology 144:2345–2353

    CAS  PubMed  Google Scholar 

  • Lugones LG, Wösten HAB, Birkenkamp KU, Sjollema KA, Zagers J, Wessels JGH (1999) Hydrophobins line air channels in fruiting bodies of Schizophyllum commune and Agaricus bisporus. Mycol Res 103:635–640

    CAS  Google Scholar 

  • Lugones LG, de Jong JF, de Vries OMH, Jalving R, Dijksterhuis J, Wösten HAB (2004) The SC15 protein of Schizophyllum commune mediates formation of aerial hyphae and attachment in the absence of the SC3 hydrophobin. Mol Microbiol 53(2):707–716

    CAS  PubMed  Google Scholar 

  • Madelin MF (1956) The influence of light and temperature on fruiting of Coprinus lagopus Fr. in pure culture. Ann Bot 20:467–480

    Google Scholar 

  • Manachère G (1980) Conditions essential for controlled fruiting of macromycetes—A review. Trans Brit Mycol Soc 75:255–270

    Google Scholar 

  • Manachère G (1988) Regulation of sporophore differentiation in some macromycetes, particularly in Coprini: An overview of some experimental studies from fruiting initiation to sporogenesis. Cryptogamie Mycol 9:291–323

    Google Scholar 

  • Matsumoto T, Kitamoto Y (1987) Induction of fruit-body formation by water-flooding treatment in sawdust cultures of Lentinus edodes. Trans Mycol Soc Jpn 28:437–443

    Google Scholar 

  • McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107(1):87–100

    CAS  PubMed  PubMed Central  Google Scholar 

  • McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4(11):1425–1433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meskauskas A, McNulty LJ, Moore D (2004) Concerted regulation of all hyphal tips generates fungal fruit body structures: experiments with computer visualizations produced by a new mathematical model of hyphal growth. Mycol Res 108:341–353

    PubMed  Google Scholar 

  • Mogensen EG, Janbon G, Chaloupka J, Steegborn C, Fu MS, Moyrand F, Klengel T, Pearson DS, Geeves MA, Buck J, Levin LR, Mühlschlegel FA (2006) Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5:103–111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moore D (1998) Fungal morphogenesis. Cambridge University Press, Cambridge

    Google Scholar 

  • Moore D, Casselton LA, Wood DA, Frankland JC (eds) (1985) Developmental biology of higher fungi. Cambridge University Press, Cambridge

    Google Scholar 

  • Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagy LG, Ohm RA, Patyshakuliyeva A, Brun A, Aerts AL et al (2012) Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci USA 109(43):17501–17506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moukha SM, Wösten HAB, Asther M, Wessels JGH (1993) In situ localization of lignin peroxidase excretion in colonies of Phanerochaete chrysosporium using sandwiched mode of culture. J Gen Microbiol 139:969–978

    CAS  PubMed  Google Scholar 

  • Mulder GH, Wessels JGH (1986) Molecular cloning of RNAs differentially expressed in monokaryons and dikaryons of Schizophyllum commune. Exp Mycol 10:214–227

    CAS  Google Scholar 

  • Muraguchi H, Kamada T (1998) The ich1 gene of the mushroom Coprinus cinereus is essential for pileus formation in fruiting. Development 125:3133–3141

    CAS  PubMed  Google Scholar 

  • Muraguchi H, Kamada T (2000) A mutation in the eln2 gene encoding a cytochrome P450 of Coprinus cinereus affects mushroom morphogenesis. Fungal Genet Biol 29:49–59

    CAS  PubMed  Google Scholar 

  • Muraguchi H, Takemaru T, Kamada K (1999) Isolation and characterization of developmental variants in fruiting using a homokaryotic fruiting strain of Coprinus cinereus. Mycoscience 40:227–235

    Google Scholar 

  • Murata Y, Fujii M, Zolan ME, Kamada T (1998) Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 149:1753–1761

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakazawa T, Miyazaki Y, Kaneko S, Shishido K (2008) Stimulative effects of light and a temperature downshift on transcriptional expressions of developmentally regulated genes in the initial stages of fruiting-body formation of the basidiomycetous mushroom Lentinula edodes. FEMS Microbiol Lett 289:67–71

    CAS  PubMed  Google Scholar 

  • Nakazawa T, Ando Y, Kitaaki K, Nakahori K, Kamada T (2011) Efficient gene targeting in ΔCc.ku70 or ΔCc.lig4 mutants of the agaricomycete Coprinopsis cinerea. Fungal Genet Biol 48:939–946

    CAS  PubMed  Google Scholar 

  • Nayak AP, Green BJ, Beezhold DH (2013) Fungal hemolysins. Med Mycol 51:1–16

    CAS  PubMed  Google Scholar 

  • Ni M, Feretzaki M, Li W, Floyd-Averette A, Mieczkowski P, Dietrich FS, Heitman J (2013) Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol 11, e1001653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niederpruem DJ (1963) Role of carbon dioxide in the control of fruiting of Schizophyllum commune. J Bacteriol 85:1300–1308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, de Vries RP, Record E, Levasseur A, Baker SE, Bartholomew KA, Coutinho PM, Erdmann S, Fowler TJ, Gathman AC, Lombard V, Henrissat B, Knabe N, Kües U, Lilly WW, Lindquist E, Lucas S, Magnuson JK, Piumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FW, vanKuyk PA, Horton JS, Grigoriev IV, Wösten HAB (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28:957–963

    CAS  PubMed  Google Scholar 

  • Ohm RA, de Jong JF, de Bekker C, Wösten HAB, Lugones LG (2011) Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation. Mol Microbiol 81:1433–1445

    CAS  PubMed  Google Scholar 

  • Ohm RA, Aerts D, Wösten HAB, Lugones LG (2013) The blue light receptor complex WC-1/2 of Schizophyllum commune is involved in mushroom formation and protection against phototoxicity. Environ Microbiol 15:943–955

    CAS  PubMed  Google Scholar 

  • Perkins JH (1969) Morphogenesis in Schizophyllum commune. I. Effects of white light. Plant Physiol 44:1706–1711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plaza DF, Lin CW, van der Velden NSJ, Aebi M, Künzler M (2014) Comparative transcriptomics of the model mushroom Coprinopsis cinerea reveals tissue-specific armories and a conserved circuitry for sexual development. BMC Genomics 15:492

    PubMed  PubMed Central  Google Scholar 

  • Purschwitz J, Müller S, Kastner C, Fischer R (2006) Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9:566–571

    CAS  PubMed  Google Scholar 

  • Purschwitz J, Müller S, Kastner C, Schöser M, Haas H, Espeso EA, Atoui A, Calvo AM, Fischer R (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18:255–259

    CAS  PubMed  Google Scholar 

  • Quiroz-Castañeda RE, Martínez-Anaya C, Cuervo-Soto LI, Segovia L, Folch-Mallol JL (2011) Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb Cell Factories 10:8

    Google Scholar 

  • Raper CA (1976) Sexuality and life cycle of the edible, wild Agaricus bitorquis. J Gen Microbiol 95:54–66

    Google Scholar 

  • Raper JR, Miles PG (1958) The genetics of Schizophyllum commune. Genetics 43:530–546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raper JR, Boyd DH, Raper CA (1965) Primary and secondary mutations at the incompatibility loci in Schizophyllum. Proc Natl Acad Sci USA 53:1324–1332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raper CA, Raper JR, Miller RE (1972) Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 64:1088–1117

    Google Scholar 

  • Raudaskoski M, Vauras R (1982) Scanning electron microscope study of fruit body differentiation in Schizophyllum commune. Trans Br Mycol Soc 78:89–96

    Google Scholar 

  • Raudaskoski M, Viitanen H (1982) Effects of aeration and light on fruit-body induction in Schizophyllum commune. Trans Br Mycol Soc 78:89–96

    Google Scholar 

  • Raudaskoski M, Yli-Mattila T (1985) Capacity for photoinduced fruiting in the dikaryon of Schizophyllum commune. Trans Br Mycol Soc 85:145–151

    Google Scholar 

  • Reijnders AFM, Stafleu JA (1992) The development of the hymenophoral trama in the Aphylophorales and Agaricales. Stud Mycol 34:1–109

    Google Scholar 

  • Ruiters MHJ, Sietsma JH, Wessels JGH (1988) Expression of dikaryon-specific mRNAs of Schizophyllum commune in relation to incompatibility genes, light, and fruiting. Exp Mycol 12:60–69

    Google Scholar 

  • Sánchez C (2010) Cultivation of Pleurotus ostreatus and other edible mushrooms. Appl Microbiol Biotechnol 85(5):1321–1337

    PubMed  Google Scholar 

  • Sánchez C, Moore D (1999) Conventional histological stains selectively stain fruit body initials of basidiomycetes. Mycol Res 103:315–318

    Google Scholar 

  • Sánchez C, Tellez-Tellez M, Diaz-Godinez G, Moore D (2004) Simple staining detects ultrastructural and biochemical differentiation of vegetative hyphae and fruit body initials in colonies of Pleurotus pulmonarius. Lett Appl Microbiol 38:483–487

    PubMed  Google Scholar 

  • Sarikaya Bayram O, Bayram O, Valerius O, Park HS, Irniger S, Gerke J, Ni M, Han KH, Yu JH, Braus GH (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6, e1001226

    PubMed  PubMed Central  Google Scholar 

  • Scholtmeijer K, de Vocht ML, Rink R, Robillard GT, Wösten HAB (2009) Assembly of the fungal SC3 hydrophobin into functional amyloid fibrils depends on its concentration and is promoted by cell wall polysaccharides. J Biol Chem 284:26309–26314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert D, Raudaskoski M, Knabe N, Kothe E (2006) Ras GTPase-activating protein Gap1 of the homobasidiomycete Schizophyllum commune regulates hyphal growth orientation and sexual development. Eukaryot Cell 5(4):683–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schuren FHJ (1999) Atypical interactions between the thn and wild-type mycelia of Schizophyllum commune. Mycol Res 103:1540–1544

    Google Scholar 

  • Schuren FHJ, Wessels JGH (1990) Two genes specifically expressed in fruiting dikaryons of Schizophyllum commune: homologies with a gene not regulated by mating-type genes. Gene 90:199–205

    CAS  PubMed  Google Scholar 

  • Schuurs TA, Dalstra HJP, Scheer JMJ, Wessels JGH (1998) Positioning of nuclei in secondary mycelium of Schizophyllum commune in relation to differential gene expression. Fungal Genet Biol 23:150–161

    CAS  PubMed  Google Scholar 

  • Schwalb MN, Miles PG (1967) Morphogenesis of Schizophyllum commune. I. Morphological variation and mating behaviour of the thin mutation. Am J Bot 54:440–446

    Google Scholar 

  • Singh RS, Bhari R, Kaur HP (2010) Mushroom lectins: current status and future perspectives. Crit Rev Biotechnol 30:99–126

    CAS  PubMed  Google Scholar 

  • Springer J, Wessels JGH (1989) A frequently occurring mutation that blocks the expression of fruiting genes in Schizophyllum commune. Mol Gen Genet 219:486–488

    CAS  Google Scholar 

  • Sun H, Zhao CG, Tong X, Qi YP (2003) A lectin with mycelia differentiation and antiphytovirus activities from the edible mushroom Agrocybe aegerita. J Biochem Mol Biol 36:214–222

    CAS  PubMed  Google Scholar 

  • Suzuki H, Vuong TV, Gong Y, Chan K, Ho C-Y, Master ER, Kondo A (2014) Sequence diversity and gene expression analyses of expansin-related proteins in the white-rot basidiomycete, Phanerochaete carnosa. Fungal Genet Biol. doi:10.1016/j.fgb.2014.05.008

    Article  PubMed  Google Scholar 

  • Swamy S, Uno I, Ishikawa T (1984) Morphogenetic effects of mutations at the A and B incompatibility factors in Coprinus cinereus. J Gen Microbiol 130:3219–3224

    Google Scholar 

  • Terashima K, Yuki K, Muraguchi H, Akiyama M, Kamada T (2005) The dst1 gene involved in mushroom photomorphogenesis of Coprinus cinereus encodes a putative photoreceptor for blue light. Genetics 171:101–108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Todd RB, Zhou M, Ohm RA, Leeggangers HACF, Visser L, de Vries RP (2014) Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics 15:240

    Google Scholar 

  • Tsusué YM (1969) Experimental control of fruit-body formation in Coprinus macrorhizus. Dev Growth Diff 11:164–178

    Google Scholar 

  • Ullrich RC, Anderson JB (1978) Sex and diploidy in Armillaria mellea. Exp Mycol 2:119–129

    Google Scholar 

  • Umar MH, van Griensven LJLD (1997) Morphogenetic cell death in developing primordia of Agaricus bisporus. Mycologia 89:274–277

    Google Scholar 

  • Uno I, Ishikawa T (1971) Chemical and genetical control of induction of monokaryotic fruiting bodies in Coprinus macrorhizus. Mol Gen Genet 113:228–239

    CAS  Google Scholar 

  • van der Valk P, Marchant R (1978) Hyphal ultrastructure in fruit body primordial of the basidiomycetes Schizophyllum commune and Coprinus cinereus. Protoplasma 95:57–72

    Google Scholar 

  • van Driel KGA, Van Peer AF, Grijpstra J, Wösten HAB, Verkleij AJ, Müller WH, Boekhout T (2008) Septal pore cap protein SPC18, isolated from the basidiomycetous fungus Rhizoctonia solani, also resides in pore plugs. Eukaryot Cell 7(10):1865–1873

    PubMed  PubMed Central  Google Scholar 

  • van Griensven LJLD (ed) (1988) The cultivation of mushrooms. Darlington Mushroom Laboratories, Rustington, Sussex

    Google Scholar 

  • van Peer AF, Müller WH, Boekhout T, Lugones LG, Wösten HAB (2009) Cytoplasmic continuity revisited: closure of septa of the filamentous fungus Schizophyllum commune in response to environmental conditions. PLoS ONE 4(6)

    Google Scholar 

  • van Peer AF, Wang F, van Driel KGA, de Jong JF, van Donselaar EG, Müller WH, Boekhout T, Lugones LG, Wösten HAB (2010) The septal pore cap is an organelle that functions in vegetative growth and mushroom formation of the wood-rot fungus Schizophyllum commune. Environ Microbiol 12(4):833–844

    PubMed  Google Scholar 

  • van Wetter MA, Wösten HAB, Wessels JGH (2000a) SC3 and SC4 hydrophobins have distinct functions in formation of aerial structures in dikaryons of Schizophyllum commune. Mol Microbiol 36:201–210

    PubMed  Google Scholar 

  • van Wetter MA, Wösten HAB, Sietsma JH, Wessels JGH (2000b) Hydrophobin gene expression affects hyphal wall composition in Schizophyllum commune. Fungal Genet Biol 31:99–104

    PubMed  Google Scholar 

  • Vidic I, Berne S, Drobne D, Maček P, Frangež R, Turk T, Štrus J, Sepčić K (2005) Temporal and spatial expression of ostreolysin during development of the oyster mushroom (Pleurotus ostreatus). Mycol Res 109(3):377–382

    CAS  PubMed  Google Scholar 

  • Watling R (1996) Patterns in fungal development - fruiting patterns in nature. In: Chiu S-W, Moore D (eds) Patterns in fungal development. Cambridge University Press, Cambridge

    Google Scholar 

  • Weber M, Salo V, Uuskallio M, Raudaskoski M (2005) Ectopic expression of a constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genet Biol 42(7):624–637

    CAS  PubMed  Google Scholar 

  • Wells K, Wells EK (eds) (1982) Basidium and basidiocarp. Springer, New York

    Google Scholar 

  • Wessels JGH (1965) Morphological and biochemical processes in Schizophyllum commune. Wentia 13:1–113

    Google Scholar 

  • Wessels JGH (1986) Cell wall synthesis in apical hyphal growth. Int Rev Cytol 104:37–79

    CAS  Google Scholar 

  • Wessels JGH (1990) Role of cell wall architecture in fungal tip growth generation. In: Heath IB (ed) Tip growth of plant and fungal cells. Academic, San Diego, pp 1–29

    Google Scholar 

  • Wessels JGH (1993) Fruiting in the higher fungi. Adv Microb Physiol 34:147–202

    CAS  PubMed  Google Scholar 

  • Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Annu Rev Phytopathol 32:413–437

    CAS  Google Scholar 

  • Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45

    CAS  PubMed  Google Scholar 

  • Wessels JGH, Marchant JR (1974) Enzymatic degradation in hyphal wall preparations from a monokaryon and a dikaryon of Schizophyllum commune. J Gen Microbiol 83:359–368

    Google Scholar 

  • Wessels JGH, Mulder GH, Springer J (1987) Expression of dikaryon-specific and non-specific mRNAs of Schizophyllum commune in relation to environmental conditions and fruiting. J Gen Microbiol 133:2557–2561

    CAS  Google Scholar 

  • Wessels JGH, de Vries OMH, Ásgeirsdóttir SA, Schuren FHJ (1991a) Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3:793–799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wessels JGH, de Vries OMH, Ásgeirsdóttir SA, Springer J (1991b) The thn mutation of Schizophyllum commune, which suppresses formation of aerial hyphae, affects expression of the Sc3 hydrophobin gene. J Gen Microbiol 137:2439–2445

    CAS  PubMed  Google Scholar 

  • Wessels JGH, Ásgeirsdóttir SA, Birkenkamp KU, de Vries OMH, Lugones LG, Scheer JMJ, Schuren FHJ, Schuurs TA, van Wetter M-A, Wösten HAB (1995) Genetic regulation of emergent growth in Schizophyllum commune. Can J Bot 73:S273–S281

    CAS  Google Scholar 

  • Wessels JGH, Schuurs TA, Dalstra HJP, Scheer JMJ (1998) Nuclear distribution and gene expression in the secondary mycelium of Schizophyllum commune. In: Gow N, Robson G, Gadd G (eds) The fungal colony. Cambridge University Press, Cambridge, pp 302–325

    Google Scholar 

  • Whitehouse HLK (1949) Multiple allelomorph heterothallism in the fungi. New Phytol 48:212–244

    Google Scholar 

  • Wiemer M, Grimm C, Osiewacz HD (2016) Molecular control of fungal senescence and longevity. In: Wendland J (ed) Growth, differentiation and sexuality. Springer, Cham, pp 155–181

    Google Scholar 

  • Woolston BM, Schlagnhaufer C, Wilkinson J, Larsen J, Shi Z, Mayer KM, Walters DS, Curtis WR, Romaine CP (2011) Long-distance translocation of protein during morphogenesis of the fruiting body in the filamentous fungus, Agaricus bisporus. PLoS ONE 6, e28412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    PubMed  Google Scholar 

  • Wösten HAB, de Vocht ML (2000) Hydrophobins, the fungal coating unravelled. Biochim Biophys Acta Rev Biomembranes 1469:79–86

    Google Scholar 

  • Wösten HAB, Wessels JGH (1997) Hydrophobins, from molecular structure to multiple functions in fungal development. Mycoscience 38:363–374

    Google Scholar 

  • Wösten HAB, Willey JM (2000) Surface active proteins enable microbial aerial hyphae to grow into the air. Microbiology 146:767–773

    PubMed  Google Scholar 

  • Wösten HAB, Moukha SM, Sietsma JH, Wessels JGH (1991) Localization of growth and secretion of proteins in Aspergillus niger. J Gen Microbiol 137:2017–2024

    PubMed  Google Scholar 

  • Wösten HAB, de Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5:1567–1574

    PubMed  PubMed Central  Google Scholar 

  • Wösten HAB, Ásgeirsdóttir SA, Krook JH, Drenth JHH, Wessels JGH (1994a) The Sc3p hydrophobin self-assembles at the surface of aerial hyphae as a protein membrane constituting the hydrophobic rodlet layer. Eur J Cell Biol 63:122–129

    PubMed  Google Scholar 

  • Wösten HAB, Schuren FHJ, Wessels JGH (1994b) Interfacial self-assembly of a hydrophobin into an amphipathic membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13:5848–5854

    PubMed  PubMed Central  Google Scholar 

  • Wösten HAB, Ruardy TG, van der Mei HC, Busscher HJ, Wessels JGH (1995) Interfacial self-assembly of a Schizophyllum commune hydrophobin into an insoluble amphipathic membrane depends on surface hydrophobicity. Coll Surf B Biointerface 5:189–195

    Google Scholar 

  • Wösten HAB, van Wetter MA, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH (1999) How a fungus escapes the water to grow into the air. Curr Biol 9:85–88

    PubMed  Google Scholar 

  • Wösten HAB, van Veluw GJ, de Bekker C, Krijgsheld P (2013) Heterogeneity in the mycelium: implications for the use of fungi as cell factories. Biotechnol Lett 35:1155–1164

    PubMed  Google Scholar 

  • Yamagishi K, Kimura T, Suzuki M, Shinmoto H (2002) Suppression of fruit-body formation by constitutively active G-protein alpha-subunits ScGP-A and ScGP-C in the homobasidiomycete Schizophyllum commune. Microbiology 148:2797–2809

    CAS  PubMed  Google Scholar 

  • Yamagishi K, Kimura T, Suzuki M, Shinmoto H, Yamaki KJ (2004) Elevation of intracellular cAMP levels by dominant active heterotrimeric G protein alpha Subunits ScGP-A and ScGP-C in homobasidiomycete, Schizophyllum commune. Biosci Biotechnol Biochem 68:1017–1026

    CAS  PubMed  Google Scholar 

  • Zhang W, Wu X, Zhou Y, Liu Z, Zhang W, Niu X, Zhao Y, Pei S, Zhao Y, Yuan S (2014) Characterization of stipe elongation of the mushroom Coprinus cinereus. Microbiology. doi:10.1099/mic.0.079418-0

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han A. B. Wösten .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Pelkmans, J.F., Lugones, L.G., Wösten, H.A.B. (2016). 15 Fruiting Body Formation in Basidiomycetes. In: Wendland, J. (eds) Growth, Differentiation and Sexuality. The Mycota, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-25844-7_15

Download citation

Publish with us

Policies and ethics