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13 The Mating-Type Genes of the Basidiomycetes

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Growth, Differentiation and Sexuality

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

Abstract

Basidiomycete mating-type genes are encoded by two different factors resulting in a tetrapolar mating system where a cross can lead to one of four different reactions, only one of which results in a fertile state. Pairs of homeodomain transcription factors termed HD1 and HD2 classes constitute one factor (b genes in the smut fungi, A genes in the hymenomycete basidiomycetes). With the evolution of basidiomycetes, pheromone/receptor (P/R) systems (a genes in smut fungi and B genes in hymenomycetes) were co-opted to become independent master regulators constituting the second factor. Subsequently, the two sets of genes underwent evolutionary radiation with duplications, inversions and gene shuffling leading to the development of multiallelic HD and P/R systems, each functioning independently of the other. The multiallelic loci each developed many allelic specificities, resulting in tens of thousands of potential mating types for some species. An additional complexity of receptor gene homologues directly involved in mate discrimination has been revealed with the ready availability of genome sequences. Using examples derived from some model species, the molecular nature of the mating-type genes, the evolution of multiallelic and multispecific mating-type loci and the potential roles of newly detected receptor-like genes are discussed.

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References

  • Aimi T, Yoshida R, Ishikawa M, Bao D, Kitamoto Y (2005) Identification and linkage mapping of the genes for the putative homeodomain protein (hox1) and the putative pheromone receptor protein homologue (rcb1) in a bipolar basidiomycete, Pholiota nameko. Curr Genet 48(3):184–194. doi:10.1007/s00294-005-0012-7

    Article  CAS  PubMed  Google Scholar 

  • Akada R, Minomi K, Kai J, Yamashita I, Miyakawa T, Fukui S (1989) Multiple genes coding for precursors of rhodotorucine A, a farnesyl peptide mating pheromone of the basidiomycetous yeast Rhodosporidium toruloides. Mol Cell Biol 9(8):3491–3498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderegg RJ, Betz R, Carr SA, Crabb JW, Duntze W (1988) Structure of Saccharomyces cerevisiae mating hormone a-factor. Identification of S-farnesyl cysteine as a structural component. J Biol Chem 263(34):18236–18240

    CAS  PubMed  Google Scholar 

  • Anderson CM, Willits DA, Kosted PJ, Ford EJ, Martinez-Espinoza AD, Sherwood JE (1999) Molecular analysis of the pheromone and pheromone receptor genes of Ustilago hordei. Gene 240(1):89–97

    CAS  PubMed  Google Scholar 

  • Asada Y, Yue CL, Wu J, Shen GP, Novotny CP, Ullrich RC (1997) Schizophyllum commune Aα mating-type proteins, Y and Z, form complexes in all combinations in vitro. Genetics 147(1):117–123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asante-Owusu RN, Banham AH, Böhnert HU, Mellor EJC, Casselton LA (1996) Heterodimerization between two classes of homeodomain proteins in the mushroom Coprinus cinereus brings together potential DNA-binding and activation domains. Gene 172(1):25–31

    CAS  PubMed  Google Scholar 

  • Badalyan SM, Polak E, Hermann R, Aebi M, Kües U (2004) Role of peg formation in clamp cell fusion of homobasidiomycete fungi. J Basic Microbiol 44(3):167–177. doi:10.1002/jobm.200310361

    Article  PubMed  Google Scholar 

  • Bakkeren G, Kämper J, Schirawski J (2008) Sex in smut fungi: structure, function and evolution of mating-type complexes. Fungal Genet Biol 45:S15–S21. doi:10.1016/j.fgb.2008.04.005

    Article  CAS  PubMed  Google Scholar 

  • Bandoni RJ (1965) Secondary control of conjugation in Tremella mesenterica. Can J Bot 43(6):627–630

    Google Scholar 

  • Banno I (1967) Studies on the sexuality of Rhodotorula. J Gen Appl Microbiol 13(16):196

    Google Scholar 

  • Banuett F, Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 86(15):5878–5882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bao D, Gong M, Zheng H, Chen M, Zhang L, Wang H, Jiang J, Wu L, Zhu Y, Zhu G, Zhou Y, Li C, Wang S, Zhao Y, Zhao G, Tan Q (2013) Sequencing and comparative analysis of the straw mushroom (Volvariella volvacea) genome. PLoS One 8(3), e58294. doi:10.1371/journal.pone.0058294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Billiard S, Lopez-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev 86(2):421–442. doi:10.1111/j.1469-185X.2010.00153.x

    Article  PubMed  Google Scholar 

  • Blakeslee AF (1904) Zygospore formation a sexual process. Science 19(492):864–866. doi:10.1126/science.19.492.864

    Article  CAS  PubMed  Google Scholar 

  • Bölker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68(3):441–450

    PubMed  Google Scholar 

  • Brown AJ, Casselton LA (2001) Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet 17(7):393–400

    CAS  PubMed  Google Scholar 

  • Casselton LA (2008) Fungal sex genes—searching for the ancestors. Bioessays 30(8):711–714. doi:10.1002/Bies.20782

    Article  CAS  PubMed  Google Scholar 

  • Casselton LA, Kües U (2007) The origin of multiple mating types in the model mushrooms Coprinopsis cinerea and Schizophyllum commune. In: Heitman J, Kronstad JW, Taylor JW, Casseleton LA (eds) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 283–300

    Google Scholar 

  • Casselton LA, Olesnicky NS (1998) Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62(1):55–70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke S (1992) Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu Rev Biochem 61:355–386. doi:10.1146/annurev.bi.61.070192.002035

    Article  CAS  PubMed  Google Scholar 

  • Coelho MA, Rosa A, Rodrigues N, Fonseca A, Goncalves P (2008) Identification of mating type genes in the bipolar basidiomycetous yeast Rhodosporidium toruloides: first insight into the MAT locus structure of the Sporidiobolales. Eukaryot Cell 7(6):1053–1061. doi:10.1128/EC.00025-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craigie JH (1927) Discovery of the function of the pycnia of the rust fungi. Nature 120:765–767

    Google Scholar 

  • Craigie JH (1931) An experimental investigation of sex in the rust fungi. Phytopathology 21:1001–1040

    Google Scholar 

  • Czaran TL, Hoekstra RF (2004) Evolution of sexual asymmetry. BMC Evol Biol 4:34. doi:10.1186/1471-2148-4-34

    Article  PubMed  PubMed Central  Google Scholar 

  • Davey J (1992) Mating pheromones of the fission yeast Schizosaccharomyces pombe: purification and structural characterization of M-factor and isolation and analysis of two genes encoding the pheromone. EMBO J 11(3):951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davey J (1998) Fusion of a fission yeast. Yeast 14(16):1529–1566, Doi: 10.1002/(SICI)1097-0061(199812)14:16<1529::AID-YEA357>3.0.CO;2-0

    CAS  PubMed  Google Scholar 

  • Davidson RC, Moore TD, Odom AR, Heitman J (2000) Characterization of the MFα pheromone of the human fungal pathogen Cryptococcus neoformans. Mol Microbiol 38(5):1017–1026

    CAS  PubMed  Google Scholar 

  • Devier B, Aguileta G, Hood ME, Giraud T (2009) Ancient trans-specific polymorphism at pheromone receptor genes in basidiomycetes. Genetics 181(1):209–223. doi:10.1534/genetics.108.093708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van de Peer Y, Rouze P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA 108(22):9166–9171. doi:10.1073/pnas.1019315108

    Article  PubMed  PubMed Central  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(5):571–589. doi:10.1128/Ec.05214-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feldbrügge M, Kämper J, Steinberg G, Kahmann R (2004) Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7(6):666–672. doi:10.1016/j.mib.2004.10.006

    Article  CAS  PubMed  Google Scholar 

  • Fell J, Statzell-Tallman A (1998) Rhodosporidium Banno. The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, The Netherlands, pp 678–692

    Google Scholar 

  • Feng Y, Davis NG (2000) Feedback phosphorylation of the yeast a-factor receptor requires activation of the downstream signaling pathway from G protein through mitogen-activated protein kinase. Mol Cell Biol 20(2):563–574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler TJ (2010) A carboxy-subterminal aromatic residue in Schizophyllum commune mating pheromones controls specific recognition by Bar4 receptor. Fungal Genet Reports 57:4–6

    Google Scholar 

  • Fowler TJ, DeSimone SM, Mitton MF, Kurjan J, Raper CA (1999) Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol Biol Cell 10(8):2559–2572

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler TJ, Mitton MF, Vaillancourt LJ, Raper CA (2001) Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics 158(4):1491–1503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler TJ, Mitton MF, Rees EI, Raper CA (2004) Crossing the boundary between the Bα and Bβ mating-type loci in Schizophyllum commune. Fungal Genet Biol 41(1):89–101

    CAS  PubMed  Google Scholar 

  • Fox HM, Burden J, Chang S-T, Peberdy JF (1994) Mating-type incompatibility between commercial strains of Lentinula edodes. Exp Mycol 18(2):95–102

    Google Scholar 

  • Fraser JA, Subaran RL, Nichols CB, Heitman J (2003) Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island, Canada. Eukaryot Cell 2(5):1036–1045

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser JA, Hsueh Y-P, Findley KM, Heitman J (2007) Evolution of the mating-type locus: the basidiomycetes. In: Heitman J, Kronstad J, Taylor J, Casselton L (eds) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 19–34

    Google Scholar 

  • Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bölker M, Kahmann R (1992) A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68(4):647–657

    CAS  PubMed  Google Scholar 

  • Giraud T, Yockteng R, Lopez-Villavicencio M, Refregier G, Hood ME (2008) Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell 7(5):765–775. doi:10.1128/EC.00440-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gola S, Kothe E (2003) The little difference: in vivo analysis of pheromone discrimination in Schizophyllum commune. Curr Genet 42(5):276–283. doi:10.1007/s00294-002-0353-4

    Article  CAS  PubMed  Google Scholar 

  • Gola S, Hegner J, Kothe E (2000) Chimeric pheromone receptors in the basidiomycete Schizophyllum commune. Fungal Genet Biol 30(3):191–196. doi:10.1006/fgbi.2000.1222

    Article  CAS  PubMed  Google Scholar 

  • Gola S, Hegner J, Kothe E (2002) Chimeric pheromone receptors in the basidiomycete Schizophyllum commune (vol 30, pg 191, 2000). Fungal Genet Biol 36(3):255–255. doi:10.1016/S1087-1845(02)00045-2

    Article  CAS  Google Scholar 

  • Griffith G, Hedger J (1994) The breeding biology of biotypes of the witches’ broom pathogen of cocoa, Crinipellis perniciosa. Heredity 72(3):278–289

    Google Scholar 

  • Groth J (1975) Two additive, independent genes for mycelial growth versus sporidial growth of haploid cultures of Ustilago hordei. Can J Bot 53(19):2233–2239

    Google Scholar 

  • Hagen DC, McCaffrey G, Sprague GF Jr (1986) Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc Natl Acad Sci USA 83(5):1418–1422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Halsall JR, Milner MJ, Casselton LA (2000) Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics 154(3):1115–1123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hegner J, Siebert-Bartholmei C, Kothe E (1999) Ligand recognition in multiallelic pheromone receptors from the basidiomycete Schizophyllum commune studied in yeast. Fungal Genet Biol 26(3):190–197. doi:10.1006/fgbi.1999.1119

    Article  CAS  PubMed  Google Scholar 

  • Heitman J, Sun S, James TY (2013) Evolution of fungal sexual reproduction. Mycologia 105(1):1–27. doi:10.3852/12-253

    Article  CAS  PubMed  Google Scholar 

  • Herskowitz I (1988) Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev 52(4):536–553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50(2):215–242

    CAS  PubMed  Google Scholar 

  • Hsueh YP, Shen WC (2005) A homolog of Ste6, the a-factor transporter in Saccharomyces cerevisiae, is required for mating but not for monokaryotic fruiting in Cryptococcus neoformans. Eukaryot Cell 4(1):147–155. doi:10.1128/EC.4.1.147-155.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsueh YP, Xue C, Heitman J (2009) A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J 28(9):1220–1233. doi:10.1038/emboj.2009.68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    CAS  PubMed  Google Scholar 

  • Hull CM, Heitman J (2002) Genetics of Cryptococcus neoformans. Annu Rev Genet 36:557–615. doi:10.1146/annurev.genet.36.052402.152652

    Article  CAS  PubMed  Google Scholar 

  • Ishibashi Y, Sakagami Y, Isogai A, Suzuki A (1984) Structures of tremerogens A-9291-I and A-9291-VIII: peptidal sex hormones of Tremella brasiliensis. Biochemistry 23(7):1399–1404

    CAS  Google Scholar 

  • James TY, Liou SR, Vilgalys R (2004) The genetic structure and diversity of the A and B mating-type genes from the tropical oyster mushroom, Pleurotus djamor. Fungal Genet Biol 41(8):813–825. doi:10.1016/j.fgb.2004.04.005

    Article  CAS  PubMed  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. doi:10.1534/genetics.105.051128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James TY, Sun S, Li W, Heitman J, Kuo HC, Lee YH, Asiegbu FO, Olson A (2013) Polyporales genomes reveal the genetic architecture underlying tetrapolar and bipolar mating systems. Mycologia 105(6):1374–1390. doi:10.3852/13-162

    Article  CAS  PubMed  Google Scholar 

  • Kamiya Y, Sakurai A, Tamura S, Takahashi N (1978) Structure of rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides. Biochem Biophys Res Commun 83(3):1077–1083

    CAS  PubMed  Google Scholar 

  • Kämper J, Reichmann M, Romeis T, Bölker M, Kahmann R (1995) Multiallelic recognition—nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81(1):73–83. doi:10.1016/0092-8674(95)90372-0

    Article  PubMed  Google Scholar 

  • Katoh K, Kuma K, Miyata T, Toh H (2005) Improvement in the accuracy of multiple sequence alignment program MAFFT. Genome Inform 16(1):22–33

    CAS  PubMed  Google Scholar 

  • Kelly M, Burke J, Smith M, Klar A, Beach D (1988) Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7(5):1537–1547

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kemp R (1974) Bifactorial incompatibility in the two-spored basidiomycetes Coprinus sassii and C. bilanatus. Trans Br Mycol Soc 62(3):547–555

    Google Scholar 

  • Kim K-H, Kang YM, Im CH, Ali A, Kim SY, Je H-J, Kim M-K, Rho HS, Lee HS, Kong W-S (2014) Identification and functional analysis of pheromone and receptor genes in the B3 mating locus of Pleurotus eryngii. PLoS One 9(8), e104693

    PubMed  PubMed Central  Google Scholar 

  • Knabe N, Jung EM, 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. doi:10.1128/Ec.00355-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kniep H (1920) Über morphologische und physiologische Geschlechtsdifferenzierung: (Untersuchungen an Basidiomyzeten). Physikal.-med Gesellschaft, Würzburg

    Google Scholar 

  • Kniep H (1922) Über Geschlechtsbestimmung und Reduktionsteilung: (Untersuchungen an Basidiomyzeten). Verlag der Physik.-Med. Ges, Würzburg

    Google Scholar 

  • Koltin Y, Raper JR, Simchen G (1967) The genetic structure of the incompatibility factors of Schizophyllum commune: the B factor. Proc Natl Acad Sci USA 57(1):55–62

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosted PJ, Gerhardt SA, Anderson CM, Stierle A, Sherwood JE (2000) Structural requirements for activity of the pheromones of Ustilago hordei. Fungal Genet Biol 29(2):107–117. doi:10.1006/fgbi.2000.1191

    Article  CAS  PubMed  Google Scholar 

  • Kothe E, Freihorst D (2012) Schleim aus Pilzen zur verbesserten Erdölförderung. BIOspektrum 18(7-12):1

    Google Scholar 

  • Kothe E, Gola S, Wendland J (2003) Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi. Curr Genet 42(5):268–275

    CAS  PubMed  Google Scholar 

  • Kües U, Casselton LA (1992a) Homeodomains and regulation of sexual development in basidiomycetes. Trends Genet 8(5):154–155

    PubMed  Google Scholar 

  • Kües U, Casselton LA (1992b) Molecular and functional analysis of the A mating type genes of Coprinus cinereus. Genet Eng 14:251–268

    Google Scholar 

  • Kües U, Navarro-Gonzalez M (2010) Mating-type orthologous genes in the primarily homothallic Moniliophthora perniciosa, the causal agent of witches’ broom disease in cacao. J Basic Microbiol 50(5):442–451. doi:10.1002/jobm.201000013

    Article  CAS  PubMed  Google Scholar 

  • Kües U, Asante-Owusu RN, Mutasa ES, Tymon AM, Pardo EH, O'Shea SF, Gottgens B, Casselton LA (1994) Two classes of homeodomain proteins specify the multiple a mating types of the mushroom Coprinus cinereus. Plant Cell 6(10):1467–1475. doi:10.1105/tpc.6.10.1467

    Article  PubMed  PubMed Central  Google Scholar 

  • Kües U, James T, Heitman J (2011) Mating type in basidiomycetes: Unipolar, bipolar, and tetrapolar patterns of sexuality. In: Pöggeler S, Wöstemeyer J (eds) The Mycota XIV: Evolution of fungi and fungal-like organisms. Springer, Berlin, Germany, pp 97–160

    Google Scholar 

  • Kwon-Chung K (1976) Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 821–833

    Google Scholar 

  • Kwon-Chung K, Bennett JE (1978) Distribution of a and α mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol 108(4):337–340

    CAS  PubMed  Google Scholar 

  • Kwon-Chung KJ, Bennett JE, Rhodes JC (1982) Taxonomic studies on Filobasidiella species and their anamorphs. Antonie van Leeuwenhoek 48(1):25–38

    CAS  PubMed  Google Scholar 

  • Lee N, Bakkeren G, Wong K, Sherwood JE, Kronstad JW (1999) The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci USA 96(26):15026–15031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SP, O'Dowd BF, Ng GY, Varghese G, Akil H, Mansour A, Nguyen T, George SR (2000) Inhibition of cell surface expression by mutant receptors demonstrates that D2 dopamine receptors exist as oligomers in the cell. Mol Pharmacol 58(1):120–128

    CAS  PubMed  Google Scholar 

  • Levasseur A, Lomascolo A, Chabrol O, Ruiz-Duenas FJ, Boukhris-Uzan E, Piumi F, Kües U, Ram AF, Murat C, Haon M, Benoit I, Arfi Y, Chevret D, Drula E, Kwon MJ, Gouret P, Lesage-Meessen L, Lombard V, Mariette J, Noirot C, Park J, Patyshakuliyeva A, Sigoillot JC, Wiebenga A, Wosten HA, Martin F, Coutinho PM, de Vries RP, Martinez AT, Klopp C, Pontarotti P, Henrissat B, Record E (2014) The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown. BMC Genomics 15:486. doi:10.1186/1471-2164-15-486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo YH, Ullrich RC, Novotny CP (1994) Only one of the paired Schizophyllum commune Aα mating-type, putative homeobox genes encodes a homeodomain essential for Aα-regulated development. Mol Gen Genet 244(3):318–324

    CAS  PubMed  Google Scholar 

  • Malloure BD, James TY (2013) Inbreeding depression in urban environments of the bird’s nest fungus Cyathus stercoreus (Nidulariaceae: Basidiomycota). Heredity 110(4):355–362. doi:10.1038/hdy.2012.95

    Article  CAS  PubMed  Google Scholar 

  • Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22(6):695–700. doi:10.1038/nbt967

    Article  CAS  PubMed  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavin JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106(6):1954–1959. doi:10.1073/pnas.0809575106

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez-Espinoza AD, Gerhardt SA, Sherwood JE (1993) Morphological and mutational analysis of mating in Ustilago hordei. Exp Mycol 17(3):200–214

    Google Scholar 

  • McClelland CM, Fu J, Woodlee GL, Seymour TS, Wickes BL (2002) Isolation and characterization of the Cryptococcus neoformans MATa pheromone gene. Genetics 160(3):935–947

    CAS  PubMed  PubMed Central  Google Scholar 

  • Metin B, Findley K, Heitman J (2010) The mating type locus (MAT) and sexual reproduction of Cryptococcus heveanensis: insights into the evolution of sex and sex-determining chromosomal regions in fungi. PLoS Genet 6(5), e1000961

    PubMed  PubMed Central  Google Scholar 

  • Michaelis S, Barrowman J (2012) Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease. Microbiol Mol Biol Rev 76(3):626–651. doi:10.1128/MMBR.00010-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore T, Edman JC (1993) The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol Cell Biol 13(3):1962–1970

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama N, Miyajima A, Arai K (1987) Common signal transduction system shared by STE2 and STE3 in haploid cells of Saccharomyces cerevisiae: autocrine cell-cycle arrest results from forced expression of STE2. EMBO J 6(1):249–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niculita-Hirzel H, Labbe J, Kohler A, le Tacon F, Martin F, Sanders IR, Kües U (2008) Gene organization of the mating type regions in the ectomycorrhizal fungus Laccaria bicolor reveals distinct evolution between the two mating type loci. New Phytol 180(2):329–342. doi:10.1111/j.1469-8137.2008.02525.x

    Article  CAS  PubMed  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 FWMR, vanKuyk PA, Horton JS, Grigoriev IV, Wosten HAB (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28(9):957–U910. doi:10.1038/Nbt.1643

    Article  CAS  PubMed  Google Scholar 

  • Olesnicky NS, Brown AJ, Dowell SJ, Casselton LA (1999) A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus. EMBO J 18(10):2756–2763. doi:10.1093/emboj/18.10.2756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olesnicky NS, Brown AJ, Honda Y, Dyos SL, Dowell SJ, Casselton LA (2000) Self-compatible B mutants in Coprinus with altered pheromone-receptor specificities. Genetics 156(3):1025–1033

    CAS  PubMed  PubMed Central  Google Scholar 

  • O'Shea SF, Chaure PT, Halsall JR, Olesnicky NS, Leibbrandt A, Connerton IF, Casselton LA (1998) A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics 148(3):1081–1090

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer GE, Horton JS (2006) Mushrooms by magic: making connections between signal transduction and fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiol Lett 262(1):1–8. doi:10.1111/j.1574-6968.2006.00341.x

    Article  CAS  PubMed  Google Scholar 

  • Parag Y (1962) Mutations in the B incompatibility factor of Schizophyllum commune. Proc Natl Acad Sci USA 48:743–750

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pelkmans JF, Lugones LG, Wösten HAB (2016) Fruiting body formation in basidiomycetes. In: Wendland J (ed) Growth, differentiation and sexuality. Springer, Heidelberg

    Google Scholar 

  • Perrin N (2012) What uses are mating types? The “developmental switch” model. Evolution 66(4):947–956. doi:10.1111/j.1558-5646.2011.01562.x

    Article  PubMed  Google Scholar 

  • Raffle V, Anderson N, Furnier G, Doudrick R (1995) Variation in mating competence and random amplified polymorphic DNA in Laccaria bicolor (Agaricales) associated with three tree host species. Can J Bot 73(6):884–890

    Google Scholar 

  • Rajchenberg M (2011) Nuclear behavior of the mycelium and the phylogeny of polypores (Basidiomycota). Mycologia 103(4):677–702. doi:10.3852/10-310

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond A (2003) Tracer: a program for analysing results from Bayesian MCMC programs such as BEAST & MrBayes. Oxford, UK. http://evolve.zoo.ox.ac.uk/software.html

  • Raper JR (1966) Genetics of sexuality in higher fungi. Ronald Press Company, New York

    Google Scholar 

  • Raper CA, Raper JR (1973) Mutational analysis of a regulatory gene for morphogenesis in Schizophyllum. Proc Natl Acad Sci USA 70(5):1427–1431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raper JR, Baxter MG, Ellingboe AH (1960) The genetic structure of the incompatibility factors of Schizophyllum commune: The A-factor. Proc Natl Acad Sci USA 46(6):833–842

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raudaskoski M (1998) The relationship between B-mating-type genes and nuclear migration in Schizophyllum commune. Fungal Genet Biol 24(1-2):207–227. doi:10.1006/fgbi.1998.1069

    Article  CAS  PubMed  Google Scholar 

  • Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9(6):847–859. doi:10.1128/Ec.00319-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raudaskoski M, Kothe E, Fowler TJ, Jung EM, Horton JS (2012) Ras and Rho small G proteins: insights from the Schizophyllum commune genome sequence and comparisons to other fungi. Biotechnol Genet Eng Rev 28:61–100

    CAS  PubMed  Google Scholar 

  • Riquelme M, Challen MP, Casselton LA, Brown AJ (2005) The origin of multiple B mating specificities in Coprinus cinereus. Genetics 170(3):1105–1119. doi:10.1534/genetics.105.040774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson CI, Kende AM, Toenjes K, Novotny CP, Ullrich RC (2002) Evidence for interaction of Schizophyllum commune Y mating-type proteins in vivo. Genetics 160(4):1461–1467

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakagami Y, Yoshida M, Isogai A, Suzuki A (1981) Peptidal sex hormones inducing conjugation tube formation in compatible mating-type cells of Tremella mesenterica. Science 212(4502):1525–1527. doi:10.1126/science.212.4502.1525

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger R, Kahmann R, Kämper J (1997) The homeodomains of the heterodimeric bE and bW proteins of Ustilago maydis are both critical for function. Mol Gen Genet 254(5):514–519

    CAS  PubMed  Google Scholar 

  • Scholtmeijer K, Cankar K, Beekwilder J, Wösten HA, Lugones LG, Bosch D (2014) Production of (+)-valencene in the mushroom-forming fungus S. commune. Appl Microbiol Biotechnol 98(11):5059–5068. doi:10.1007/s00253-014-5581-2

    Article  CAS  PubMed  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. doi:10.1128/Ec.5.4.683-695.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz B, Banuett F, Dahl M, Schlesinger R, Schafer W, Martin T, Herskowitz I, Kahmann R (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60(2):295–306

    CAS  PubMed  Google Scholar 

  • Seike T, Yamagishi Y, Iio H, Nakamura T, Shimoda C (2012) Remarkably simple sequence requirement of the M-factor pheromone of Schizosaccharomyces pombe. Genetics 191(3):815–825. doi:10.1534/genetics.112.140483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen GP, Park DC, Ullrich RC, Novotny CP (1996) Cloning and characterization of a Schizophyllum gene with Aβ6 mating-type activity. Curr Genet 29(2):136–142

    CAS  PubMed  Google Scholar 

  • Skrede I, Maurice S, Kauserud H (2013) Molecular characterization of sexual diversity in a population of Serpula lacrymans, a tetrapolar basidiomycete. G3 3(2):145–152. doi:10.1534/g3.112.003731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Specht CA (1995) Isolation of the Bα and Bβ mating-type loci of Schizophyllum commune. Curr Genet 28(4):374–379

    CAS  PubMed  Google Scholar 

  • Specht CA, Novotny CP, Ullrich RC (1992a) Mitochondrial DNA of Schizophyllum commune: restriction map, genetic map, and mode of inheritance. Curr Genet 22(2):129–134

    CAS  PubMed  Google Scholar 

  • Specht CA, Stankis MM, Giasson L, Novotny CP, Ullrich RC (1992b) Functional analysis of the homeodomain-related proteins of the Aα locus of Schizophyllum commune. Proc Natl Acad Sci USA 89(15):7174–7178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spellig T, Bölker M, Lottspeich F, Frank RW, Kahmann R (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13(7):1620–1627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spit A, Hyland RH, Mellor EJC, Casselton LA (1998) A role for heterodimerization in nuclear localization of a homeodomain protein. Proc Natl Acad Sci USA 95(11):6228–6233. doi:10.1073/pnas.95.11.6228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stankis MM, Specht CA (2007) Cloning the mating-type genes of Schizophyllum commune: a historical perspective. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC, USA, pp 267–282

    Google Scholar 

  • Stankis MM, Specht CA, Yang H, Giasson L, Ullrich RC, Novotny CP (1992) The Aα mating locus of Schizophyllum commune encodes two dissimilar multiallelic homeodomain proteins. Proc Natl Acad Sci USA 89(15):7169–7173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stanton BC, Hull CM (2007) Mating-type locus control of cell identity. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 59–73

    Google Scholar 

  • Szabo Z, Tonnis M, Kessler H, Feldbrügge M (2002) Structure-function analysis of lipopeptide pheromones from the plant pathogen Ustilago maydis. Mol Genet Genomics 268(3):362–370. doi:10.1007/s00438-002-0756-4

    Article  CAS  PubMed  Google Scholar 

  • Takano H, Onoue K, Kawano S (2010) Mitochondrial fusion and inheritance of the mitochondrial genome. J Plant Res 123(2):131–138. doi:10.1007/s10265-009-0268-y

    Article  CAS  PubMed  Google Scholar 

  • Vaillancourt LJ, Raudaskoski M, Specht CA, Raper CA (1997) Multiple genes encoding pheromones and a pheromone receptor define the Bβ1 mating-type specificity in Schizophyllum commune. Genetics 146(2):541–551

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vallim MA, Fernandes L, Alspaugh JA (2004) The RAM1 gene encoding a protein-farnesyltransferase β-subunit homologue is essential in Cryptococcus neoformans. Microbiology 150(Pt 6):1925–1935. doi:10.1099/mic.0.27030-0

    Article  CAS  PubMed  Google Scholar 

  • van Peer AF, Park SY, Shin PG, Jang KY, Yoo YB, Park YJ, Lee BM, Sung GH, James TY, Kong WS (2011) Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS One 6(7), e22249. doi:10.1371/journal.pone.0022249

    Article  CAS  PubMed  PubMed Central  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. doi:10.1016/j.fgb.2005.03.012

    Article  CAS  PubMed  Google Scholar 

  • Wendland J, Vaillancourt LJ, Hegner J, Lengeler KB, Laddison KJ, Specht CA, Raper CA, Kothe E (1995) The mating-type locus Bα1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J 14(21):5271–5278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehouse H (1949) Heterothallism and sex in the fungi. Biol Rev 24(4):411–447

    CAS  PubMed  Google Scholar 

  • Wong GJ, Wells K (1985) Modified bifactorial incompatibility in Tremella mesenterica. Trans Br Mycol Soc 84(1):95–109

    Google Scholar 

  • Wu L, van Peer A, Song W, Wang H, Chen M, Tan Q, Song C, Zhang M, Bao D (2013) Cloning of the Lentinula edodes B mating-type locus and identification of the genetic structure controlling B mating. Gene 531(2):270–278. doi:10.1016/j.gene.2013.08.090

    Article  CAS  PubMed  Google Scholar 

  • Yi R, Mukaiyama H, Tachikawa T, Shimomura N, Aimi T (2010) A-mating-type gene expression can drive clamp formation in the bipolar mushroom Pholiota microspora (Pholiota nameko). Eukaryot Cell 9(7):1109–1119. doi:10.1128/EC.00374-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue CL, Osier M, Novotny CP, Ullrich RC (1997) The specificity determinant of the Y mating-type proteins of Schizophyllum commune is also essential for Y-Z protein binding. Genetics 145(2):253–260

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors very much appreciate the comments and help regarding MrBayes/phylogenetic analysis of Dr. M. Gube and D. Sammer, and we also thank the latter for providing protein data on T. vaccinum. We also would like to gratefully acknowledge the Graduate School JSMC and the Deutsche Forschungsgemeinschaft for funding.

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Authors and Affiliations

  1. Institute for Microbiology, Microbial Communication, Friedrich Schiller University Jena, Neugasse 25, 07743, Jena, Germany

    Daniela Freihorst & Erika Kothe

  2. Department of Biological Sciences, Southern Illinois University Edwardsville, 1651, Edwardsville, IL, 62026, USA

    Thomas J. Fowler

  3. Department of Biology, Sacred Heart University, 5151 Park Avenue, Fairfield, CT, 06825, USA

    Kirk Bartholomew

  4. Department of Biochemistry, Plant Molecular Biology, University of Turku, Biocity A, Tykistök. 6A, 20520, Turku, Finland

    Marjatta Raudaskoski

  5. Department of Biological Sciences, Union College, Peter Irving Wold Center, Schenectady, NY, 12308, USA

    J. Stephen Horton

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  1. Daniela Freihorst
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  3. Kirk Bartholomew
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  4. Marjatta Raudaskoski
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  6. Erika Kothe
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Correspondence to Erika Kothe .

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  1. Carlsberg Laboratory, Yeast Genetics, Copenhagen V, Denmark

    Jürgen Wendland

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Freihorst, D., Fowler, T.J., Bartholomew, K., Raudaskoski, M., Horton, J.S., Kothe, E. (2016). 13 The Mating-Type Genes of the 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_13

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