Abstract
We summarize current knowledge on the structure of mating type loci in different species of basidiomycetes, giving special consideration to bipolar and tetrapolar heterothallic species. In all three subphyla of the Basidiomycota, heterothallic bipolar, heterothallic tetrapolar, and homothallic species have been described, and in all subphyla, there are evidently also anamorphic (asexual) species. Generally, a multitude of different insights on mating type genes and their evolution have now been revealed in different basidiomycete species using both model and non-model species and molecular and evolutionary genetics. The existing data suggest that multiple mating types have evolved only once in fungi, being restricted to Basidiomycota. We introduce a new term, unipolarity, to describe the unisexual mode of fungal reproduction that is distinguished from the bipolar and tetrapolar configurations. The existence of facultative unipolarity within heterothallic species may have been largely ignored in the past but merits further investigation.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbate JL, Hood ME (2010) Dynamic linkage relationships to the mating-type locus in automictic fungi of the genus Microbotryum. J Evol Biol 23:1800–1805
Abe K (1987) Differentiation of mating tubes induced by the mating hormone Rhodotorucine A during the mitotic cycle of Rhodosporidium toruloides. J Gen Appl Microbiol 33:437–444
Abe K, Kusaka I, Fukui S (1975) Morphological change in the early stages of the mating process of Rhodosporidium toruloides. J Bacteriol 122:710–718
Aimi T, Yoshida R, Ishikawa M, Bao DP, Kitamoto Y (2005) Identification and linkage mapping of the putative homeodomain protein (hox1) and the putative pheromone receptor homologue (rcb1) in a bipolar basidiomycete, Pholiota nameko. Curr Genet 48:184–194
Akada R, Minomi K, Yamashiata I, Miyakawa T, Fukui S (1987) Cloning of a gene coding for Rhodotorucine A, a farnesyl peptide mating pheromone of Rhodosporidium toruloides. Agric Biol Chem 51:1211–1215
Akada R, Kaj J, Yamashita I, Miyakawa T, Fukui S (1989a) Genomic organization of multiple genes coding for Rhodotorucine A, a lipopeptide mating pheromone of the basidiomycetous yeast Rhodosporidium toruloides. Arch Microbiol 152:484–487
Akada R, Minomi K, Kai J, Yamashita I, Miyakawa T, Fukui S (1989b) Multiple genes coding for precursors of Rhodotorucine A, a farnesyl peptide mating pheromone of the basidiomycetous yeast Rhodosporidium toruloides. Mol Cell Biol 9:3491–3498
Albert HH, Schenck S (1996) PCR amplification from a homolog of the bE mating-type gene as a sensitive assay for the presence of Ustilago scitaminea DNA. Plant Dis 80:1189–1192
Alby K, Schaefer D, Bennett RJ (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460:890–893
Alic M, Gold, MH (1985) Genetic recombination in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 50:27–30
Alic M, Letzring C, Gold MH (1987) Mating system and basidiospore formation in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Env Microbiol 53:1464–1469
Allen RF (1932) A cytological study of heterothallism in Puccinia triticina. J Agric Res 44:733–753
Allen RF (1934) A cytological study of heterothallism in Puccinia sorghi. J Agric Res 49:1047–1069
Alspaugh JA, Perfect JR, Heitman J (1998) Signal transduction pathways regulating differentiation and pathogenicity of Cryptococcus neoformans. Fungal Genet Biol 25:1–14
Anderson CM, Willits DA, Kosted PJ, Ford E, Martinez-Espinoza AD, Sherwood JE (1999) Molecular analysis of the pheromone and pheromone receptor genes of Ustilago hordei. Gene 240:89–97
Anikster Y, Eilam T, Mittelman L, Szabo LJ, Bushnell WR (1999) Pycnial nectar of rust fungi induces cap formation on pycniospores of opposite mating type. Mycologia 91:858–870
Anikster Y, Eilam T, Bushnell WR (2000) Interspecific transfer of pycnial nectar induces pycniospore caps in rust fungi in a manner related to mating type within species. Mycol Res 104:311–316
Arcangioli B, Thon G (2004) Mating-type cassettes: structure, switching and silencing. In: Egel R (ed) The molecular biology of Schizosaccharomyces pombe. Springer, Berlin Heidelberg New York, pp 129–148
Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. BioEssays 27:76–85
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 vivo. Genetics 147:117–123
Asante-Owusu RN, Banham AH, Böhnert HU, Mellor EJ, Casselton LA (1996) Heterodimerization between two classes of homeodomain proteins in the mushroom Coprinus cinereus brings together potential DNA-binding and activation domains. Gene 172:25–31
Ásgeirsdóttir SA, Schuren FHJ, Wessels JGH (1994) Assignment of genes to pulse-field separated chromosomes of Schizophyllum commune. Mycol Res 98:689–693
Bachtrog D (2006) A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16:578–585
Bachtrog D (2008) The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179:1513–1525
Badalyan S, Polak E, Hermann R, Aebi M, Kües U (2004) Role of peg formation in clamp cell fusion of homobasidiomycete fungi. J Basic Microbiol 44:167–177
Badrane H, May G (1999) The divergence-homogenization duality in the evolution of the b1 mating type gene of Coprinus cinereus. Mol Biol Evol 16:975–986
Bai F-Y, Zhao J-H, Takashima M, Jia J-H, Boekhout T, Nakase T (2002) Reclassification of the Sporobolomyces roseus and Sporidiobolus pararoseus complexes, with the description of Sporobolomyces phaffii sp. nov. Int J Syst Evol Microbiol 52:2309–2314
Bakkeren G, Kronstad JW (1993) Conservation of the b-mating-type gene-complex among bipolar and tetrapolar smut fungi. Plant Cell 5:123–136
Bakkeren G, Kronstad JW (1994) Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci 91:7985–7089
Bakkeren G, Kronstad JW (1996) The pheromone cell signalling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143:1601–1613
Bakkeren GM, Kronstad JW (2007) Bipolar and tetrapolar mating systems in the Ustilaginales. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 389–404
Bakkeren G, Gibbard B, Yee A, Froeliger E, Leong S, Kronstad J (1992) The a and b loci of Ustilago maydis hybridize with DNA sequences from other smut fungi. Mol Plant Microb Interact 5:347–355
Bakkeren G, Jiang G, Warren RL, Butterfield Y, Shin H, Chiu R, Linning R, Schein J, Lee N, Hu G, Kupfer DM, Tang Y, Roe BA, Jones S, Marra M, Kronstad JW (2006) Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet Biol 43:655–666
Bakkeren G, Kämper J, Schirawski J (2008) Sex in smut fungi: Structure, function and evolution of mating–type compleses. Fungal Genet Biol 45:S15–S21
Banham AH, Asante-Owusu RN, Göttgens B, Thompson SAJ, Kingsnorth CD, Mellor EJC, Casselton LA (1995) An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell 7:773–783
Bandoni RJ (1963) Conjugation in Tremella mesenterica. Can J Bot 41:467–474
Banno I (1967) Studies on sexuality of Rhodotorula. J Gen Appl Microbiol 13:167–196
Banuett F (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Ann Rev Genet 29:179–208
Banuett F (2007) History of mating types in Ustilago maydis. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 351–388
Banuett F, Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Exp Mycol 18:247–266
Barres B, Halkett F, Dutech C, Andrieux A, Pinon J, Frey P (2008) Genetic structure of the poplar rust fungus Melampsora larici-populina: Evidence for isolation by distance in Europe and recent founder effects overseas. Infect Genet Evol 8:577–587
Barsoum E, Sjöstrand JOO, Åström SU (2010) Ume6 is required for the MAT a/MATα cellular identity and transcriptional silencing in Kluyveromyces lactis. Genetics 184:999–1011
Basse C, Farsing JW (2006) Promoters and their regulation in Ustilago maydis and other phytopathogenic fungi. FEMS Microbiol Lett 254:208–216
Bensaude M (1918) Recherches sur le cycle évolutif et la sexualité chez les Basidiomycètes. PhD thesis, Faculté des Sciences de Paris, Imprimerie Nemourienne, Henri Bouloy, Nemours, France
Billiard S, López-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 86:421–442
Blakeslea AF (1904) Zygospore formation a sexual process. Science 3:864–866
Bloomfield G, Skelton J, Ivens A, Tanakqa Y, Kay RR (2010) Sex determination in the social amoeba Dictyostelium discoideum. Science 330:1533–1536
Boidin J, Lanquentin P (1984) Le genre Amylostereum (Basidiomycetes) incompatibilités partielles entre espèces allopartriques. Bull Trimest Soc Mycol Fr 100:211–236
Bölker M (1998) Sex and crime: Heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25:143–156
Bölker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signalling components. Cell 68:441–450
Boulton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575
Brachmann A, Weinzierl G, Kämper J, Kahmann R (2001) Identification of genes of the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42:1047–1063
Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Ann Rev Phytopathol 47:423–445
Brown AJ, Casselton LA (2001) Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet 17:393–400
Bui T, Lin X, Malik R, Heitman J, Carter D (2008) Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, α mating type populations. Eukaryot Cell 7:1771–1780
Buller AHR (1950) Researches on fungi. Vol. VII. The sexual process in the Uredinales. University of Toronto Press, Toronto, Canada
Bürglin T (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nuc Acids Res 25:4173–4180
Burt A (2000) Sex, recombination, and the efficiency of selection – was Weismann right? Evolution 54:337–351
Butler G, Kenny C, Fagan A, Kurischko C, Gaillardin C, Wolfe KH (2004) Evolution of the MAT locus and its HO endonuclease in yeast species. Proc Natl Acad Sci USA 101:1632–1637
Butlin R (2002) Evolution of sex: the costs and benefits of sex: new insights from old asexual lineages. Nat Rev Genet 3:311–317
Byrnes EJ III, Li W, Lewit Y, Perfect JR, Carter DA, Cox GM, Heitman J (2010) First reported case of Cryptococcus gattii in the Southeastern USA: Implications for travel-associated acquisition of an emerging pathogen. PLoS ONE 4:5851
Caldwell GA, Naider F, Becker JM (1995) Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation. Microbiol Rev 59:406–422
Casselton LA (2008) Fungal sex genes – searching for the ancestors. BioEssays 30:711–714
Casselton LA, Challen MP (2006) The mating types of the basidiomycetes. In: Kües U, Fischer R (eds) The Mycota, vol. 1, 2nd edn. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 357–374
Casselton LA, Kües U (1994) Mating-type genes in homobasidiomycetes. In: Wessels JGH, Meinhard F (eds) The Mycota, vol. 1. Growth, differentiation, and sexuality. Springer, Berlin Heidelberg New York, pp 307–321
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, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 283–300
Casselton LA, Olesnicky ND (1998) Molecular genetics of mating type recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62:55–70
Chang YC, Wickes BL, Miller GF, Penoyer LA, Kwon-Chung KJ (2000) Cryptococcus neoformans STE12α regulates virulence but is not essential for mating. J Exp Med 191:871–881
Chang YC, Penoyer LA, Kwon-Chung KJ (2001) The second STE12 homologue of Cryptococcus neoformans is MATa-specific and plays an important role in virulence. Proc Natl Acad Sci USA 98:3258–3263
Chang YC, Miller GF, Kwon-Chung KJ (2003) Importance of a developmentally regulated pheromone receptor of Cryptococcus neoformans for virulence. Infect Immun 71:4953–4960
Chang YC, Wright LC, Tscharke RL, Sorrell TC, Wilson CF, Kwon-Chung KJ (2004) Regulatory roles for the homeodomain and C2H2 zinc finger regions of Cryptococcus neoformans STE12αp. Mol Microbiol 53:1385–1396
Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Ann Rev Genet 23:251–287
Chaturvedi V, Fan J, Stein B, Behr MJ, Samsonoff WA, Wickes BL, Chaturvedi S (2002) Molecular genetic analyses of mating pheromones reveal intervariety mating of hybridization in Cryptococcus neoformans. Infect Immun 70:5225–5235
Chen P, Sapperstein SK, Choi JD, Michaelis S (1997) Biogenesis of the Saccharomyces cerevisiae mating pheromone a-factor. J Cell Biol 136:251–259
Chung S, Karos M, Chang YC, Lukszo J, Wickes BL, Kwon-Chung KJ (2002) Molecular analysis of CPRα, a MATα-specific pheromone receptor gene of Cryptococcus neoformans. Eukaryot Cell 1:432–439
Clarke DL, Woodlee GL, McClelland CM, Seymour TS, Wickes BL (2001) The Cryptococcus neoformans STE11α gene is similar to other fungal mitogen-activated protein kinase kinase (MAPKKK) genes but is mating type specific. Mol Microbiol 40:200–213
Coelho MA, Rosa A, Rodriguez N, Fonseca Á, Gonçalves P (2008) Identification of mating type genes in the bipolar basidiomycetous yeast Rhodosporidium toruloides: First insight into the MAT locus structure of the genus Sporidiobolales. Eukaryot Cell 7:1053–1061
Coelho MA, Sampaio JP, Gonçalves P (2010) A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet 6:e1001052
Coppin E, Debuchy R, Arnaise S, Picard M (1997) Mating types and sexual development in filamentous ascomycetes. Microbiol Mol Biol Rev 61:411–428
Craigie JH (1927) Discovery of the function of the pycnia of the rust fungi. Nature 120:765–67
Craigie JH (1931) An experimental investigation of sex in the rust fungi. Phytopathol 21:101–1040
Cubeta MA, Vilgalys R (1997) Population biology of the Rhizoctonia solani complex. Phytopathol 7:480–484
Davey J, Davis K, Hughes M, Ladds G, Powner D (1998) The processing of yeast pheromones. Sem Cell Dev Biol 9:19–30
Davidson RC, Moore TDE, Odom AR, Heitman J (2000) Characterization of the MFα pheromone of the human fungal pathogen Cryptococcus neoformans. Mol Microbiol 38:1017–1026
Davidson RC, Nichols CBN, Cox GM, Perfect JR, Heitman J (2003) A MAP kinase cascade composed of cell type specific and non-specific elements controls mating and differentiation of the fungal pathogen Cryptococcus neoformans. Mol Microbiol 49:469–485
Daud F, Napiah I (1991) Mating systems of two Auricularia spp. in Malyasia. Malyasian Appl Biol 20:87–91
Day AW (1979) Mating type and morphogenesis in Ustilago violacea. Bot Gaz 140:94–109
Day PR (1960) The structure of the A mating type locus in Coprinus lagopus. Genetics 45:641–650
Derelle R, Lopez P, Le Guyaser H, Manuel M (2007) Homeodomain proteins belong to the ancestral toolkit of eukaryotes. Evol Dev 9:212–219
Devier B, Aguileta G, Hood M, Giraud T (2009) Ancient trans-specific polymorphism at pheromone receptor genes in basidiomycetes. Genetics 181:209–223
Devier, B, Aguileta G, Hood ME, Giraud T (2010) Using phylogenies of pheromone receptor genes in Microbotryum violaceum species complex to investigate possible speciation by hybridization. Mycologia 102:689–696
Dhawale SS, Kessler K (1993) Alternative methods for production and staining of Phanerochaete chrysosporium basidiospores. Appl Environ Microbiol 59:1675–1677
Dhitaphichit P, Nawawongwiwat J (2006) Mating system of five edible species of the mushroom, genus Lentinus. Songklanakarin J Sci Technol 28:285–292
Dolgin ES, Charlesworth B (2006) The fate of transposable elements in asexual populations. Genetics 174:817–827
Duboule D (1994) Guidebook to homeobox genes. Oxford University Press, Oxford, UK
Dunthorn M, Katz LA (2010) Secretive ciliates and putative asexuality in microbial eukaryotes. Trends Microbiol 18:183–188
Duplessis S, Cuomo CA, Lin Y-P, 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, Maho 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, RouzÕ P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F (2011) Obligate biotrophy features inraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA, doi:10.1073/pnas.1019315108
Dyer PS (2008) Evolutionary biology: Genomic clues to original sex in fungi. Curr Biol 18:R207–R209
Ekena JL, Stanton BC, Schiebe-Owens JA, Hull CM (2008) Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factor Sxi1α and Sxi2a. Eukaryot Cell 7:48–57
Esser K (2000) Kryptogamen 1. Cyanobakterien Algen Pilze Flechten, 3rd edn. Springer, Berlin Heidelberg New York
Esser K, Meinhardt F (1977) Common genetic control of dikaryotic and monokaryotic fruiting in the basidiomycete Agrocybe aegerita. Mol Gen Genet 155:113–115
Esser K, Saleh F, Meinhardt F (1979) Genetics of fruit body production in higher basidiomycetes. 2. Monokaryotic and dikaryotic fruiting in Schizophyllum commune. Curr Genet 1:85–88
Fedler M, Luh KS, Stelter K, Nieto-Jacobo F, Basse CW (2009) The a2 mating-type locus genes lga2 and rga2 direct uniparental mitochondrial DNA (mtDNA) inheritance and constrain mtDNA recombination during sexual development of Ustilago maydis. Genetics 181:847–860
Feldbrügge M, Kämper J, Steinberg G, Kahmann R (2004) Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7:666–672
Feldbrügge M, Bölker M, Steinberg G, Kämper J, Kahmann R (2006) Regulatory and structural networks orchestrating mating, dimorphism, cell shape, and pathogenesis in Ustilago maydis. In: Kües U, Fischer R (eds) The mycota. Vol. 1, 2nd edn. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 375–392
Fell JW, Statzell Tallman A (1981) Heterothallism in the basidiomycetous yeast genus Sporidiobolus Nyland. Curr Microbiol 5:77–82
Fell JW, Statzell-Tallman A (1998) Rhodosporidium Banno. In: Kurtzman CP and Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 678–692
Findley K, Rodriguez-Carres M, Metin B, Kroiss J, Fonseca Á, Vilgalys R, Heitman J (2009) Phylogeny and phenotypic characterization of pathogenic Cryptococcus species and closely related saprobic taxa in the Tremellales. Eukaryot Cell 8:363–361
Fowler TJ, Vaillancourt LJ (2007) Pheromones and pheromone receptors in Schizophyllum commune mate recognition: Retrospective of a half-century of progress and a look ahead. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 301–316
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 10:2559–2572
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 158:1491–1503
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 41:89–101
Fox HM, Burden J, Chang S-T, Pederby JF (1994) Mating-type incompatibility between commercial strains of Lentinula edodes. Exp Mycol 18:95–102
Frankel C, Ellingboe AH (1977) New mutations and a 7-chromosome map of Schizophyllum commune. Genetics 85:417–425
Franzot SP, Hamdan JS, Currie BP, Casadevall A (1997) Molecular epidemiology of Cryptococcus neoformans in Brazil and the United States: evidence for both local genetic differences and a global clonal population structure. J Clin Microbiol 35:2243–2251
Fraser JA, Heitman J (2005) Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev 15:645–651
Fraser JA, Subaran RL, Nichols CB, Heitman LJ (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 2:1036–1045
Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, Dietrich FS, Heitman J (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2:2243–2255
Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, Diezmann S, Allen A, Stajich JE, Dietrich FS, Perfect JR, Heitman J (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360–1364
Fraser JA, Hsueh Y-P, Fundley KM, Heitman J (2007) Evolution of the mating-type locus: the basidiomycetes. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 19–34
Froeliger EH, Leong SA (1991) The a mating-type alleles of Ustilago maydis are idiomorphs. Gene 100:113–122
Fuchs U, Hause G, Schuchardt I, Steinberg G (2006) Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 18:2066–2081
Fuller RS, Sterne RE, Thorner J (1988) Enzymes required for yeast prohormone processing. Ann Rev Physiol 50:345–362
Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868
Garcia-Muse T, Steinberg G, Perez-Martin J (2003) Pheromone-induced G2 arrest on the phytopathogenic fungus Ustilago maydis. Eukaryot Cell 2:494–500
Gerard PR, Husson C, Pinon J, Frey P (2006) Comparison of genetic and virulence diversity of Melampsora larici-populina populations on wild and cultivated poplar and influence of the alternate host. Phytopathology 96:1027–1036
Gieser PT, May G (1994) Comparison of 2 b1 alleles from within the A-mating-type of the basidiomycete Coprinus cinereus. Gene 146:167–176
Gillissen B, Bergemann J, Sandmann C, Schröer B, Bölker M, Kahmann R (1992) A 2-component regulatory system for self non-self recognition in Ustilago maydis. Cell 68:647–657
Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME (2008) Mating system of the anther smut fungus Microbotryum violaceum: Selfing under heterothallism. Eukaryot Cell 7:765–775
Gola S, Kothe E (2003a) The little difference: in vivo analysis of pheromone discrimination in Schizophyllum commune. Curr Genet 42:276–283
Gola S, Kothe E (2003b) An expression system for the functional analysis of pheromone genes in the tetrapolar basidiomycete Schizophyllum commune. J Basic Microbiol 43:104–112
Gola S, Hegner J, Kothe E (2000) Chimeric pheromone receptors in the basidiomycete Schizophyllum commune. Fungal Genet Biol 30:191–196
Gold MH, Alic M (1993) Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiol Rev 57:605–622
Golubev W (1993) Rhodosporidium babjevae, a new heterothallic yeast species (Ustilaginales). Syst Appl Microbiol 16:445–449
Graul RC, Sadée W (2001) Evolutionary relationships among G protein-coupled receptors using a clustered database approach. AAPS PharmSci 3:12
Griffiths GW, Hedger JN (1994) The breeding biology of biotypes of the witches´ broom pathogen of cocoa, Crinipellis perniciosa. Heredity 72:278–289
Groth JV (1975) Two additive, independent genes for mycelial growth versus sporidial growth of haploid cultures of Ustilago hordei. Can J Bot 53:2233–2239
Gryganski AP, Lee SC, Litvintseva AP, Smith ME, Bonito G, Porter TM, Anishchenko IM, Heitman J, Vilgalys R (2010) Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS ONE 5:e12273
Haber JE (2007) Decisions, decisions: Donor preference during budding yeast mating-type switching. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 159–170
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 154:1115–1123
Hartmann HA, Kahmann R, Bölker M (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J 15:1632–1642
Hegner J, Siebert–Bartholmei C, Kothe E (1999) Ligand recognition on multiallelic pheromone receptors from the basidiomycete Schizophyllum commune studied in yeast. Fungal Genet Biol 26:190–197
Heimel K, Scherer M, Schuler D, Kämper J (2010a) The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signalling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 22:2908–2922
Heimel K, Scherer M, Vranes M, Wahl R, Pothiratana C, Schuler B, Voncon V, Finkernagel F, Flor-Parra I, Kämper J (2010) The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PloS Pathog 6:e1001035
Heitman J (2009) Microbial genetics: Love the one you’re with. Nature 460:807–808
Heng HHQ (2007) Elimination of altered karyotypes by sexual reproduction preserves species identity. Genome 50:517–524
Herskowitz I (1988) Life-cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev 52:536–553
Herskowitz I (1989) A regulatory hierarchy for cell specialization in yeast. Nature 342:749–757
Hibbett DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbusch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Rous C, Ryvarden L, Sampaio JP, Schüssler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A high-level phylogenetic classification of the fungi. Mycol Res 111:509–547
Hiremath SS, Chowdhary A, Kowshik T, Randhawa HS, Sun S, Xu J (2008) Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiol 154:1513–1524
Hiscock SJ, Kües U (1999) Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int Rev Cytol 193:165–295
Hoffmann JA, Kendrick EL (1969) Genetic control of compatibility in Tilletia controversa. Phytopathol 59:79–83
Holton CS, Kendrick EL (1957) Fusion between secondary sporidia in culture as a valid index of sex compatibility in Tilletia caries. Phytopathol 47:688–89
Hood ME (2002) Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160:457–461
Hood ME (2005) Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:1–10
Hood ME, Antonovics J (2004) Mating within the meiotic tetrad and the maintenance of genomic heterozygosity. Genetics 166:1751–1759
Hood ME, Antonovics J, Koskella B (2004) Shared forces of sex chromosome evolution in haploids and diploids. Genetics 168:141–146
Hsueh Y-P, Heitman J (2008) Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr Opin Microbiol 11:617–524
Hsueh Y-P, Shen W-C (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 4:147–255
Hsueh Y-P, Idnurm A, Heitman J (2006) Recombination hotspots flank the Cryptococcus mating-type locus: Implications for the evolution of a fungal sex-chromosome. PLoS Genet 2:e184
Hsueh Y-P, Xue C, Heitman J (2007) G protein signaling governing cell fate decisions involves opposing Gα subunits in Cryptococcus neoformans. Mol Biol Cell 18:3237–3249
Hsueh Y-P, Fraser JA, Heitman J (2008) Transitions in sexuality: Recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans. Eukaryot Cell 7:1847–1855
Hsueh Y-P, Xue C, Heitman J (2009) A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J 28:1220–1233
Hsueh Y-P, Metin B, Findley K, Rodriguez-Carres, Heitman J (2011) The mating-type locus of Cryptococcus: evolution of gene clusters governing sex determination and sexual reproduction from phylogenomic perspective. In: Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadavall A (eds) Cryptococcus: From human pathogen to model yeast. ASM Press, Washington, DC, pp 139–149
Hull CM, Heitman J (2002) Genetics of Cryptococcus neoformans. Ann Rev Genet 36:557–615
Hull CM, Davidson RC, Heitman J (2002) Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1α. Genes Dev 16:3046–3060
Hull CM, Cox GM, Heitman J (2004) The α-specific cell identity factor Sxi1α is not required for virulence of Cryptococcus neoformans. Infect Immun 72:3643–3645
Hull CM, Boily MJ, Heitman J (2005) Sex-specific homeodomain proteins Sxi1α and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot Cell 4:526–535
Hurst LD (1996) Why are there only two sexes? Proc R Soc Lon Ser B Biol Sci 263:415–422
Huyer G, Kistler A, Nouvel FJ, George CM, Boyte ML, Michaelis S (2006) Saccharomyces cerevisiae a-factor mutants reveals residues criticical for processing, activity, and export. Eukaryot Cell. 5:1560–1570
Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3:e95
Idnurm A Bahn YS, Nielsen K, Lin X, Fraser JA, Heitman J (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nature Rev Microbiol 3:753–764
Idnurm A, James TY, Vilgalys R (2007) Sex in the rest: Mysterious mating in the Chytridiomycota and Zygomycota. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 407–418
Idnurm A, Walton FJ, Floyd A, Heitman J (2008) Identification of the sex genes in an early diverged fungus. Nature 451:193–196
Imai Y, Yamamoto M (1994) The fission yeast mating pheromone P-factor: its molecular structure, gene structure and physiological activities to induce gene expression and G1 arrest in the mating partner. Genes Dev 8:328–338
Isaya G, Sakati WR, Rollins RA, Shen GP, Hanson LC, Ullrich RC, Novotny CP (1995) Mammalian mitochondrial intermediate peptidase: Structure/function analysis of a new homolog from Schizophyllum commune and relationship to thimet oligopeptidases. Genomics 28:450–461
Ishibashi Y, Sakagami Y, Isogai A, Suziki A (1984) Structures of tremerogens A-9291-I and A-9291-VIII. Peptidyl sex hormones of Tremella brasiliensis. Biochemistry 23:1399–1404
James TY, Kües U, Rehner SA, Vilgalys R (2004a) Evolution of the gene encoding mitochondrial intermediate peptidase and its cosegregation with the A mating-type locus of mushroom fungi. Fungal Genet Biol 41:381–390
James TY, Liou SR, Vilgalys R (2004b) The genetic structure and diversity of the A and B mating-type genes from the tropical oyster mushroom, Pleurotus djamor. Fungal Genet Biol 41:813–825
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 172:1877–1891
James TY, Lee M, van Diepen LTA (2011) A single mating-type locus comprised of homeodomain genes promotes nuclear migration and heterokaryosis in the white-rot fungus Phanerochaete chrysosporium. Eukaryot Cell 10:249–261
Josefsson L-G (1999) Evidence for kinship between diverse G-protein coupled receptors. Gene 239:333–340
Judson OP, Nordmark BB (1996) Ancient asexual scandals. Trends Ecol Evol 1:11:41–46
Julian MC, Dullemans AM, van Silfthout CH, Keijer J (1997) Nuclear behaviour in homokaryotic and heterokaryotic fruiting of Thanatephorus cucumeris (Rhizoctonia solani) anastomosis group 1, subgroup IC. Mycologia 89:361–374
Kaffarnik F, Müller P, Leibundgut M, Kahmann R, Feldbrügge M (2003) PKA and MAPK phosporylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22:5817–5826
Kahmann R, Kämper J (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytol 164:31–42
Kahmann R, Schirawski J (2007) Mating in the smut fungi: From a to b to the downstream cascades. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 377–387
Kamiya Y, Sakarai A, Tamura S, Abe K, Tsuchiya E, Fukui S (1977) Isolation and chemical characterization of peptidyl factor controlling mating tube formation in Rhodosporidium toruloides. Agric Biol Chem 41:1099–1100
Kamiya Y, Sakurai A, Tamura S, Takahashi N, Abe K, Tsuchiya E, Fukui S (1978a) Amino-acid sequence of rhodotorucine-A, a peptidyl factor controlling mating tube formation in Rhodosporidium toruloides. Agric Biol Chem 42:209–211
Kamiya Y, Sakurai A, Tamura S, Takahashi N, Abe K, Tsuchiya E, Fukui S (1978b) Isolation of rhodotorucine A, a peptidyl factor inducing mating tube formation in Rhodosporidium toruloides. Agric Biol Chem 42:1239–1243
Kamiya Y, Sakurai A, Tamura S, Takahashi N, Abe K, Tsuchiya E, Fukui S, Kitada C, Fujino (1978c) Structure of rhodotorucine-A, a novel lipopeptide inducing mating tube formation in Rhodosporidium. Biochem Biophys Res Com 83:1077–1083
Kamiya Y, Sakurai A, Tamura S, Tsuchiya E, Abe K, Fujui S (1979) Structure of rhodotorucine-A, a peptidyl factor, inducing mating tube formation in Rhodosporidium toruloides. Agric Biol Chem 43:363–369
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 81:73–83
Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, Perlin MH, Wösten HAB, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Münch K, Rössel N, Scherer M, Vraneš M, Ladendorf O, Voncon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alsonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Schwimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal pathogen Ustilago maydis. Nature 444:97–101
Karos M, Chang YC, McClelland CM, Clarke DL, Fu J, Wickes BL, Kwon-Chung KJ (2000) Mapping of the Cryptococcus neoformans MATα locus: Presence of mating type-specific mitogen-activated protein cascade homologs. J Bacteriol 182:6222–6227
Kemp ROF (1974) Bifactorial incompatibility in the two-spored basidiomycetes Coprinus sassii and Coprinus bilanatus. Trans Br Mycol Soc 62:547–555
Kidd SE, Guo H, Bartlett KH, Xu J, Kronstad JW (2005) Comparative gene genealogies indicate that two clonal lineages of Cryptococcus gattii in British Columbia resemble strains from other geographical areas. Eukaryot Cell 4:1629–1638
Kirk PM, Cannon PF, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CABI, Wallingford, UK
Kniep H (1928) Die Sexualität der niederen Pflanzen. Fischer, Jena, Germany
Kollmorgen JF, Trione EJ (1980) Mating-type interactions between sporidia of the wheat-bunt fungus Tilletia caries. Can J Bot 58:1994–2000
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 57:55–62
Koltin Y, Stamberg J, Lemke PA (1972) Genetic structure and evolution of the incompatibility factors in higher fungi. Bacteriol Rev 36:156–171
Koppitz M, Spellig T, Kahmann R, Kessler H (1996) Lipoconjugates: Structure–activity studies for pheromone analogues of Ustilago maydis with varied lipophilicity. Int J Peptide Protein Res 48:377–390
Kosted PJ, Gerhardt SA, Anderson CM, Stierle A, Sherwood JE (2000) Structural requirements for activity of the pheromones of Ustilago hordei. Fungal Genet Biol 29:107–117
Kothe E (1996) Tetrapolar fungal mating types: Sexes by the thousands. FEMS Microbiol Rev 18:65–87
Kothe E (1999) Mating types and pheromone recognition in the basidiomycete Schizophyllum commune. Fungal Genet Biol 27:146–152
Kothe E (2001) Mating-type genes for basidiomycete strain improvement in mushroom farming. Appl Microbiol Biotechnol 56:602–612
Kothe E, Raudaskoski M (2010) Basidiomycete mating type genes and pheromone signalling. Eukaryot Cell 9:847–859
Kothe E, Gola S, Wendland J (2003) Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi. Curr Genet 42:268–275
Krejĉí R, Homolka L (1991) Genetic mapping in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Env Microbiol 57:151–156
Kronstad JW, Leong SA (1990) The b mating type locus of Ustilago maydis contains variable and constant regions. Genes Dev 4:1384–1395
Kronstad JW, Staben C (1997) Mating type in filamentous fungi. Ann Rev Microbiol 31:245–276
Kruzel EK, Hull CM (2010) Establishing an unusual cell type: how to make a dikaryon. Curr Opin Microbiol 13:706–711
Kües U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353
Kües U, Casselton LA (1992) Homeodomains and regulation of sexual development in basidiomycetes. Trends Genet 8:154–155
Kües U, Casselton LA (1993) The origin of multiple mating types in mushrooms. J Cell Sci 104:227–230
Kües U, Navarro-González M (2009) Communication of fungi on individual, species, kingdom, and above kingdom level. In: Anke T, Weber D (eds) The Mycota, Vol 15. Physiology and genetics, selected basic and applied aspects. Springer, Berlin, pp 79–106
Kües U, Navarro-González M (2010) Mating-type orthologous genes in the primarily homothallic Moniliophthora perniciosa, the causal agent of Witches’ Broom Disease in cacao. J Basic Microbiol 50:442–451
Kües U, Richardson WVJ, Tymon AM, Mutasa ES, Göttgens B, Gaubatz S, Gregoriades A, Casselton LA (1992) The combination of dissimilar alleles of the Aα and Aβ gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus. Genes Dev 6:568–577
Kües U, Asante-Owusu RN, Mutasa ES, Tymon AM, Pardo EH, O´Shea SF, Göttgens B, Casselton LA (1994a) Two classes of homeodomain proteins specify the multiple A mating types of the mushroom Coprinus cinereus. Plant Cell 6:1467–1475
Kües U, Göttgens B, Stratmann R, Richardson WSJ, ÓShea SF, Casselton LA (1994b) A chimeric homeodomain protein causes self compatibility and constitutive sexual development in the mushroom Coprinus cinereus. EMBO J 13:4054–4059
Kües U, Tymon AM, Richardson WVJ, May G, Gieser PT, Casselton LA (1994c) A mating type factors of Coprinus cinereus have variable numbers of specificity genes encoding 2 classes of homeodomains. Mol Gen Genet 245:45–52
Kües U, Granado JD, Hermann R, Boulianne RP, Kertesz-Chaloupková K, Aebi M (1998) The A mating type and blue light regulate all known differentiation processes in the basidiomycete Coprinus cinereus. Mol Gen Genet 260:81–91
Kües U, James TY, Vilgalys R, Challen MP (2001a) The chromosomal region containing pab-1, mip, and the A mating type locus of the secondary homothallic homobasidiomycete Coprinus bilanatus. Curr Genet 39:16–24
Kües U, Klaus MJ, Polak E, Aebi M (2001b) Multiple cotransformations in Coprinus cinereus. Fungal Genet Newslett 48:32–34
Kües U, Polak E, Bottoli APF, Hollenstein M, Walser PJ, Boulianne RP, Hermann R, Aebi M (2002a) Vegetative development in Coprinus cinereus. In: Osiewacz HD (ed) Molecular biology of fungal development. Marcel Dekker, New York, pp 133–164
Kües U, Walser PJ, Klaus MJ, Aebi M (2002b) Influence of activated A and B mating-type pathways on developmental processes in the basidiomycete Coprinus cinereus. Mol Gen Genom 268:262–271
Kües U, Künzler M, Bottoli APF, Walser PJ, Granado JD, Liu Y, 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 Publishers (India), Jodhpur, India, pp 431–470
Kurjan J, Herskowitz I (1982) Structure of a yeast pheromone gene (MFα): a putative α-factor precursor contains four tandem copies of mature α-factor. Cell 30:933–943
Kwon-Chung KJ (1975) A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67:1197–1200
Kwon-Chung KJ (1976a) Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 67:821–833
Kwon-Chung KJ (1976b) Morphogenesis of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 68:821–833
Kwon-Chung KJ, Bennett JE (1978) Distribution of α and a mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol 108:337–340
Labarère J, Noël T (1992) Mating type switching in the tetrapolar basidiomycete Agrocybe aegerita. Genetics 131:307–319
Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967
Lawrence GJ (1980) Multiple mating-type specificities in the flax rust Melampsora lini. Science 209:501–503
Lee H, Chang YC, Kwon-Chung KJ (2005) TUP1 disruption reveals biological differences between MATa and MATα strains of Cryptococcus neoformans. Mol Microbiol 55:1222–1232
Lee H, Chang YC, Varma A, Kwon-Chung KJ (2009) Regulatory diversity of TUP1 in Cryptococcus neoformans. Eukaryot Cell 8:1901–1908
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 96:15026–15031
Lee SC, Corradi N, Doan S, Dietrich F, Keeling PJ, Heitman J (2010a) Evolution of the sex-related locus and genomic features hsraed in microsporidia and fungi. PLoS One 5:e10539
Lee SC, Ni M, Li W, Shertz C, Heitman J (2010b) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74:298–340
Lemke PA (1969) A reevaluation of homothallism, heterothallism, and the species concept in Sistotrema brinkmannii. Mycologia 61:57–76
Lengeler KB, Davidson RC, D’Souza C, Harashima T, Shen WC, Wang P, Pan XW, Waugh M, Heitman J (2000a) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785
Lengeler KB, Wang P, Cox GM, Perfect JR, Heitman J (2000b) Identification of the MAT a mating-type locus of Cryptococcus neoformans reveals a serotype A MAT a strain thought to have been extinct. Proc Natl Acad Sci USA 97:14455–14460
Lengeler 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 1:704–718
Li AZ, Xu XF, Lin FX, Cheng SM, Lin FC (2007) Cloning and identification of partial DNA fragment for the B mating-type factor in Lentinula edodes using degenerate PCR. World J Microbiol Biotechnol 23:411–415
Li L, Shen G, Zhang ZG, Wang YL, Thompson JK, Wang P (2007) Canonical heteromeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol Biol Cell 18:4201–4209
Lin X (2009) Cryptococcus neoformans: Morphogenesis, infection, and evolution. Infect Genet Evol 9:401–416
Lin X, Heitman J (2006) The biology of the Cryptococcus neoformans species complex. Ann Rev Microbiol 60:69–105
Lin X, Heitman J (2007) Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 35–58
Lin X, Hull CM, Heitman J (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:1017–1021
Lin X, Huang JC, Mitchell TG, Heitman J (2006) Virulence attributes and hyphal growth of C. neoformans are quantitative traits and the MATα allele enhances filamentation. PLoS Genet 2:e187
Lin X, Litvintseva AP, Nielsen K, Patel S, Floyd A, Mitchell TG, Heitman J (2007) αADα hybrids of Cryptococcus neoformans: Evidence of same sex mating in nature and hybrid fitness. PLoS Genet 3:1975–1990
Lin X, Patel S, Litvintseva AP, Floyd A, Mitchell TG, Heitman J (2009) Diploids in the Cryptococcus neoformans serotype A population homozygous for the α mating type originate via unisexual mating. PLoS Pathogens 5:e1000283
Lin X, Jackson JC, Feretzaki M, Xue C, Heitman J (2010) Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and same-sex mating in Cryptococcus neoformans. PLoS Genet 6:e1000953
Litvintseva AP, Marra RE, Nielsen K, Heitman J, Vilgalys RJ, Mitchell TG (2003) Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell 2:1162–1168
Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG (2006) Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (serotype A), including a unique population in Botswana. Genetics 172:2223–2238
Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF (2009) Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9:11
Lukens L, Yicun H, May G (1996) Correlation of genetic and physical maps at the A mating-type locus of Coprinus cinereus. Genetics 144:1471–1477
Luo XC, Cheng LG (1989) Sexuality and formation of monokaryotic fruitbody in Auricula auricula and Auricularia auricula. Mushroom J Trop 9:12–28
Mahlert M, Vogler C, Stelter K, Hause G, Basse CW (2009) The a2 mating-type-locus gene lga2 of Ustilago maydis interferes with mitochondrial dynamics and fusion, partially in dependence on a Dnm1-like fission component. J Cell Sci 122:2402–2412
Martinez D, Larrondo LF, Putnam N, Gelpke MDS, 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. Nature Biotech 22:695–700
Martinez D, Challacome 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, Lavon 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, Lucash S, Salamov A, Shapiro H, Tu H, Chee CL, Mira 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 of the wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959
Martinez-Espinoza AD, Gerhardt SA, Sherwood JE (1993) Morphological and mutational analysis of mating in Ustilago hordei. Exp Mycol 17:200–214
May G, Matzke R (1995) Recombination and variation at the A mating-type of Coprinus cinereus. Mol Biol Evol 12:794–802
May G, Le Chevanton L, Pukkila PJ (1991) Molecular analysis of the Coprinus cinereus mating type-A factor demonstrates an unexpectedly complex structure. Genetics 128:529–538
May G, Shaw F, Badrane H, Vekemans X (1999) The signature of balancing selection: fungal mating compatibility gene evolution. Proc Natl Acad Sci USA 96:9172–9177
McClelland CM, Fu J, Woodlee GL, Seymour TS, Wickes BL (2002) Isolation and characterisation of the Cryptococcus MATa pheromone gene. Genetics 160:935–947
McClelland CM, Chang YC, Varma A, Kwon-Chung KJ (2004) Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol 12:208–212
McCusker JH (2006) Saccharomyces cerevisiae: an emerging and model pathogenic fungus. In: Heitman J, Filler SG, Edwards JE, Mitchell AP (eds) Molecular principles of fungal pathogenesis. ASM Press, Washington, DC, pp 245–259
McLaughlin DJ, Hibbett DS, Lutzoni F, Spatafora JW, Vilgalys R (2009) The search for the fungal tree of life. Trends Microbiol 17:488–497
Meinhardt F, Esser K (1990) Sex determination and sexual differentiation in filamentous fungi. Crit Rev Plant Sci 9:329–341
Mendoza-Mendoza A, Eskova A, Weise C, Czajkowski R, Kahmann R (2009) Hpa2 regulates the pheromone response transcription factor prf1 in Ustilago maydis. Mol Microbiol 72:683–698
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:e1000961
Metzenberg RL, Glass NL (1990) Mating type and mating strategies in Neurospora. BioEssays 12:53–59
Miyakawa T, Miyama R, Tabata M, Tsuchiya E, Fukui S (1985a) A study on the biosynthesis of tremerogen A-10, a polyisoprenyl peptide mating pheromone of Tremella mesenterica, using an inhibitor of mevalonate synthesis. Agric Biol Chem 49:1343–1347
Miyakawa T, Tabata M, Tsuchiya E, Fukui S (1985b) Biosynthesis and secretion of tremerogen A-10, a polyisoprenyl peptide mating pheromone of Tremella mesenterica. Eur J Biochem 147:489–493
Mondego JMC, Carazzolle MF, Costa GGL, Formighieri EF, Parizzi LP, Rincones J, Cotomacci C, Carraro DM, Cunha AF, Carrer H, Vidal RO, Estrela RC, García O, Thomazella DPT, de Oliviera BV, Pires ABL, Rio MCS, Araújo MRR, de Morares MH, Castro LAB, Gramachi KP, Gonçalves MS, Moura Neto JP, Góes Neto A, Barbosa LV, Guiltinan MJ, Bailey BA, Meinhardt LW, Cascardo LCM, Pereira GAG (2008) A genome survey of Moniliophthora perniciosa insights into Witches´ Broom Disease of cacao. BMC Genomics 9:548
Morrow CA, Fraser JA (2009) Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res 9:161–177
Moore TD, Edman JC (1993) The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol Cell Biol 13:1962–1970
Mukherjee K, Brocchieri L, Bürglin TR (2009) A comparative classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794
Murata Y, Kamada T (2009) Identification of new mutant alleles of pcc1 in the homobasidiomycete Coprinopsis cinerea. Mycoscience 50:137–139
Murata Y, Fujii M, Zolan M, Kamada T (1998) Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 149:1753–1761
Mutasa ES, Tymon AM, Göttgens B, Mellon FM, Little PFR, Casselton LA (1990) Molecular organization of an A-mating type factor of the basidiomycete fungus Coprinus cinereus. Curr Genet 18:233–229
Naider F, Becker JM (2004) The α-factor mating pheromone of Saccharomyces cerevisiae: a model for studying the interaction of peptide hormones and G-coupled receptor. Peptides 25:1441–1463
Narisawa K, Yamaoka Y, Katsuya K (1995) Mating type of isolates derived from the spermogonial state of Puccinia coronata var. coronata. Mycoscience 35:131–135
Neiman M, Meirmans S, Meirmans PG (2009) What can asexual lineages tell us about the maintenance of sex? Ann NY Acad Sci 1168:185–200
Nichols CB, Fraser JA, Heitman J (2004) PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating on Cryptococcus neoformans. Mol Biol Cell 15:4476–4489
Niculita-Hirzel H, Labbé 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 180:329–342
Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, Heitman, J (2003) Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and α isolates. Infect Immun 71:4831–4841
Nielsen K, De Obaldia AL, Heitman J (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6:949–959
Nielsen O, Egel R (2007) The mat genes of Schizosaccharomyces pombe: Expression, homothallic switch, and silencing. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 143–158
Nobles MK (1943) A contribution towards a clarification of the Trametes serialis complex. Can J Res C 21:211–234
North J (1990) Linkage map of Coprinus cinereus (Schaeff. ex Fr.) S.F.Gray. In: O´Brien SJ (ed) Genetic maps. Book 3. Lower eukaryotes. Fifth edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 3.70–3.81
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, Magnusson JK, Oiumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FWMR, vanKuyk PA, Horton JS, Grigoriev IV, Wösten HAB (2010) Formation of mushrooms and lignocellulose degradation in the genome sequence of Schizophyllum commune. Nat Biotechnol 28:957–963
Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, New York, NY
Okabayashi K, Kano R, Watanabe T, Hasegawa A (2006) Serotypes and mating types of clinical isolates from feline cryptococcosis in Japan. J Vet Med Sci 68:91–94
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 18:2756–2763
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 156:1025–1033
Ongay-Larios L, Navarro-Olmes R, Kawasaki L, Velázquez-Zavala N, Sánchez-Paredes E, Torres-Quiroz F, Coello G, Coria R (2007) Kluyveromyces lactis sexual pheromones. Gene structures and cellular responses to α-factor. FEMS Yeast Res 7:740–747
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 148:1081–1090
Panwar SL, Legrand M, Dignard D, Whiteway M, Magee PT (2003) MFα 1, the gene encoding the α mating pheromone of Candida albicans. Eukaryot Cell 2:1350–1360
Pardo EH, O´Shea SF, Casselton LA (1996) Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes. Genetics 144:87–94
Park Y-D, Panepinto J, Sin S, Larsen P, Giles S, Williamson PR (2010) Mating pheromone in Cryptococcus is regulated by a transcriptional/degradative “futile” cycle. J Biol Chem 285:34746–34756
Pei MH, Bayon C, Ruiz C, Tubby I (2007) Population structure of poplar rust Melampsora larici-populina in the UK inferred from AFLP. Plant Pathol 56:472–479
Piepenbring M, Stoll M, Oberwinkler F (2002) The generic position of Ustilago maydis, Ustilago scitaminea, and Ustilago esculenta (Ustilaginales). Mycol Prog 1:71–80
Phadke SS, Zufall RA (2009) Rapid diversification of mating systems in ciliates. Biol J Linn Soc 98:187–197
Pöggeler S (2007) MAT and its role in homothallic ascomycete Sordaria macrospora. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 171–188
Puhalla JE (1970) Genetic studies of the b incompatibility locus of Ustilago maydis. Genet Res 16:229–232
Qu P, Aratani A, Syoji T, Toda T, Kubota M, Hyakumachi M (2008a) Use of single-protoplast isolates in the study of the mating phenomena of Rhizoctonia solani (Thanatephorus cucumeris) AG-1 IC and IA. Mycoscience 49:132–137
Qu P, Yamashita K, Toda T, Priyatmojo A, Kubota M, Hyakumachi M (2008b) Heterokaryon formation in Thanatephorus cucumeris (Rhizoctonia solani) AG-1 IC. Mycol Res 112:1088–1100
Raeder UW, Thompson W, Broda P (1989) RFLP-based genetic map of Phanerochaete chrysosporium ME446: lignin peroxidase genes occur in clusters. Mol Microbiol 3:911–918
Raper CA (1990) Schizophyllum commune. In: O´Brien SJ (ed) Genetic maps. Book 3. Lower eukaryotes. Fifth edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 3.90–3.91
Raper CA (1998) Schizophyllum commune, a model for genetic studies of the Basidiomycetes. In: Sidhu GS (ed) Genetics of plant pathogenic fungi. Academic Press, London, UK, pp 511–522
Raper JR (1966) Genetics of sexuality of higher fungi. Ronald Press, New York, NY
Raper JR, Flexer AS (1971) Mating systems and evolution of the basidiomycetes. In: Petersen RH (ed) Evolution of the higher basidiomycetes. University of Tennessee Press, Knoxville, Tennessee, pp 149–167
Raper JR, Krongelb (1958) Genetic and environmental aspects of fruiting in Schizophyllum commune Fr. Mycologia 50:707–740
Raper JR, Baxter MG, Middleton RB (1958) The genetic structure of the incompatibility loci in Schizophyllum. Proc Natl Acad Sci USA 44:889–900
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: 833–842
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
Raudaskoski M (1998) The relationship between B-mating-type genes and nuclear migration in Schizophyllum commune. Fungal Genet Biol 24:207–227
Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bölker M, Kahmann R (1997) G proteins in Ustilago maydis: Transmission of multiple signals? EMBO J 16:1934–1942
Ren P, Roncaglia P, Springer DJ, Fan J, Chaturvedi V (2005) Genomic organization and expression of 23 new genes from MATα locus of Cryptococcus neoformans var. gattii. Biochim Biophys Res Commun 326:233–241
Ren P, Springer DJ, Behr MJ, Samsonoff WA, Chaturvedi S, Chaturvedi V (2006) Transcription factor STE12α has distinct roles in morphogenesis, virulence, and ecological fitness of the primary pathogenic yeast Cryptococcus gattii. Eukaryot Cell 5:1065–1080
Riquelme M, Challen MP, Casselton LA, Brown AJ (2005) The origin of multiple B mating specificities in Coprinus cinereus. Genetics 170:1105–1119
Robertson CI, Kende AM, Toenjes K, Novotny CP, Ullrich RC (2002) Evidence for interaction of Schizophyllum commune Y mating-type proteins in vivo. Genetics 160:1461–1467
Rodriguez-Carres M, Findley K, Sun S, Dietrich FS, Heitman J (2010) Morphological and genomic characterization of Filobasidiella depauperata: A homothallic sibling species of the pathogenic Cryptococcus species complex. PLoS ONE 5:e9620
Romeis T, Kämper J, Kahmann R (1997) Single-chain fusions of two unrelated homeodomain proteins trigger pathogenicity in Ustilago maydis. Proc Natl Acad Sci USA 94:1230–1234
Romeis T, Brachmann A, Kahmann R, Kämper J (2000) Identification of a target gene for the bE-bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37:54–66
Rusche LN, Rine J (2010) Switching the mechanism of mating type switching: a domesticated transposase supplants a domesticated homing endonuclease. Genes Dev 24:10–14
Rydholm C, Dyer PS, Lutzoni F (2007) DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell 6:868–874
Sakagami Y, Isogai A, Suzuki S, Tamara S, Kitada C, Fujino M (1979) Structure of tremerogen A-10, a peptidyl hormone inducing conjugation tube formation in Tremella mesenterica. Agric Biol Chem 43:2643–2645
Sakagami Y, Yoshida M, Isogai A, Suzuki A (1981a) Peptidal sex hormones inducing conjugation tube formation in compatible mating-type cells of Tremella mesenterica. Science 212:1525–1527
Sakagami Y, Yoshida M, Isogai A, Suzuki A (1981b) Structure of tremerogen a-13, a peptidyl hormone of Tremella mesenterica. Agric Biol Chem 45:1045–1047
Saracli MA, Yildiran ST, Sener K, Gonlum A, Doganci L, Keller SM, Wickes BL (2006) Genotyping of Turkish environmental Cryptococcus neoformans var. neoformans isolates by pulsed field gel electrophoresis and mating type. Mycoses 49:124–129
Saul N, Krockenberger M, Carter D (2008) Evidence of recombination in mixed-mating-type and α-only populations of Cryptococcus gattii sourced from single Eucalyptus tree hollows. Eukaryot Cell 7:727–734
Schirawski J, Heinze B, Wagenknecht M, Kahmann R (2005) Mating type loci of Sporisorium reilianum: novel pattern with three a and multiple b specificities. Eukaryot Cell 4:1317–1327
Schlesinger R, Kahmann R, Kämper J (1997) The homeodomain of the heterodimeric bE and bW proteins of Ustilago maydis are both critical for function. Mol Gen Genet 254:514–519
Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer 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 60:295–306
Shen G-P, Park DC, Ullrich RC, Novotny CP (1996) Characterization of a Schizophyllum gene with Aβ6 mating-type activity. Curr Genet 29:136–142
Shen G-P, Chen Y, Song D, Peng Z, Novotny CP, Ullrich RC (2001) The Aα6 locus: its relation to mating-type regulation of sexual development in Schizophyllum commune. Curr Genet 39:340–345
Shen WC, Davidson RC, Cox GM, Heitman J (2002) Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans. Eukaryot Cell 1:366–377
Sherwood JE, Kosted PJ, Anderson CM, Gerhardt SA (1998) Production of a mating inhibitor of Ustilago hordei. Phytopathol 88:456–464
Silva J (1972) Alleles at the b incompatibility locus in Polish and North American populations of Ustilago maydis (CD) Corda. Physiol Plant Pathol 2:333–337
Snetselaar KM, Bölker M, Kahmann R (1996) Ustilago maydis mating hyphae orient their growth toward pheromone sources. Fungal Genet Biol 20:299–312
Specht CA (1995) Isolation of the Bα and Bβ mating-type loci of Schizophyllum commune. Curr Genet 28:374–379
Specht CA, Stankis MM, Giasson L, Novotny CP, Ullrich RC (1992) Functional analysis of the homeodomain-related proteins of the Aα locus of Schizophyllum commune. Proc Natl Acad Sci 89:7174–7178
Specht CA, Stankis MM, Novotny CP, Ullrich RC (1994) Mapping the heterogeneous DNA region that determines the 9 Aα-mating-type specificities of Schizophyllum commune. Genetics 137:709–714
Spellig T, Bölker M. Lottspeich F, Frank RW, Kahmann R (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13:1620–1627
Spiers AG, Hopcroft DH (1994) Comparative studies of the poplar rusts Melampsora medusae, M. larici-populina and their interspecific hybrid M. medusae-populina. Mycol Res 98:889–903
Spit A, Hyland RH, Mellor EJ, Casselton LA (1998) A role for heterodimerization in nuclear localization of a homeodomain protein. Proc Natl Acad Sci USA 95:6228–6233
Srivilai P (2006) Molecular analysis of genes acting in fruiting body development in basidiomycetes. PhD thesis, Georg-August-University Göttingen, Göttingen, Germany
Stahl U, Esser K (1976) Genetics of fruit body production in higher basidiomycetes. 1. Monokaryotic fruiting and its correlation with dikaryotic fruiting in Polyporus ciliatus. Mol Gen Genet 148:183–197
Stajich JS, Wilke SK, Ahrén D, Au CH, Birren BW, Borodovsky M, Burns C, Canbäck B, Casselton LA, Cheng CK, Deng J, Dietrich FS, Fargo DC, Farman ML, Gathman AC, Goldberg J, Guigo R, Hoegger PJ, Hooker JB, Huggins A, James TY, Kamada T, Kilaru S, Kodira C, Kües U, Kupfer D, Kwan HS, Lomsadze A, Li W, Lilly WW, Ma L-J, Mackey AJ, Manning G, Martin F, Muraguchi H, Natvig DO, Palmeri H, Ramesh MA, Rehmeyer CJ, Roe BA, Shenoy N, Stanke M, Ter-Hovhannisyan V, Tunlid A, Velagapudi R, Vision TJ, Zeng Q, Zolan ME, Pukkila PJ (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci USA107:11655–11665
Stankis MM, Specht CA, Yang HL, Giasson L, Ullrich RC, Novotny CP (1992) The Aα mating locus of Schizophyllum commune encodes 2 dissimilar multiallelic homeodomain proteins. Proc Natl Acad Sci USA 89:7169–7173
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 59–74
Stanton BC, Giles SS, Kruzel EK, Warren CL, Ansari AZ, Hull CM (2009) Cognate site identifier analysis reveals novel binding properties of the sex inducer homeodomain proteins of Cryptococcus neoformans. Mol Microbiol 72:1334–1347
Statzell-Tallman A, Fell JW (1998) Sporidiobolus Nyland. In: Kurtzman CP and Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, The Netherlands, pp 693–699
Statzell-Tallman A, Belloch C, Fell JW (2008) Kwoniella mangroviensis gen. nov, sp. nov. (Tremellales, Basidiomycota), a teleomorphic yeast from mangrove habitats in the Florida Everglades and Bahamas. FEMS Yeast Res 8:103–113
Stoll M, Begerow D, Oberwinkler F (2005) Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109:342–356
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
Takemaru T (1961) Genetical study on fungi. XI. The mating system in Lentinus edodes. Rep Tottori Mycol Inst 1:61–68
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetic analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tetsuka Y, Katsuya K (1984) Mating experiments of isolates derived from the spermogonial state of Gymnosporangium asiaticum. Proc Japan Acad 60, Ser B:149–152
Thompson W, Broda P (1987) Mating behaviour in an isolate of Phanerochaete chrysosporium. Trans Br Mycol Soc 89:285–294
Toda T, Hyakumach M (2006) Heterokaryon formation in Thanetophorus cucumeris anastomosis group 2-2IV. Mycologia 98:726–736
Tokimoto K, Komatsu M, Takemaru T (1973) Incompatibility factors in the natural population of Lentinus edodes in Japan. Rep Tottori Mycol Inst 10:371–376
Trail F, Mills D (1990) Growth of haploid Tilletia strains in planta and genetic analysis of a cross of Tilletia caries X T. controversa. Phytopathol 80:367–370
Tscharke RL, Lazera M, Chang YC, Wickes BL, Kwon-Chung KJ (2003) Haploid fruiting in Cryptococcus neoformans is not mating type α-specific. Fungal Genet Biol 39:230–237
Tsuchiya E, Fukui S (1987) Binding of Rhodotorucine A, a lipopeptidyl mating hormone, to A cells of Rhodosporidium toruloides for induction of sexual differentiation. Biochem Biophys Res Comm 85:473–479
Turgeon G, Debuchy R (2007) Cochliobolus and Podospora: Mechanism of sex determination and the evolution of reproductive life style. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi. Molecular determination and evolutionary implications. ASM Press, Washington, DC, pp 93–122
Tymon AM, Kües U, Richardson WVJ, Casselton LA (1992) A fungal mating type protein that regulates sexual and asexual development contains a POU-related domain. EMBO J 11:1805–1813
Ullrich RC, Raper JR (1975) Primary homothallism – Relation to heterothallism in the regulation of sexual morphogenesis in Sistotrema. Genetics 80:311–321
Urban M, Kahmann R, Bölker M (1996a) The biallelic a mating type locus of Ustilago maydis: Remnants of an additional pheromone gene indicate evolution from a multiallelic ancestor. Mol Gen Genet 250:414–420
Urban M, Kahmann R, Bölker M (1996b) Identification of the pheromone response element in Ustilago maydis. Mol Gen Genet 251:31–37
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 146:541–551
Valério E, Gadanho M, Sampaio JP (2008a) Reappraisal of the Sporobolomyces roseus species complex and description of Sporidiobolus metaroseus sp. nov. Int J Syst Evol Microbiol 58:736–741
Valério E, Gadanho M, Sampaio JP (2008b) Sporidiobolus johnsonii and Sporidiobolus salmenicolor revisited. Mycol Prog 7:125–131
van der Nest MA, Slippers B, Stenlid J, Wilken PM, Vasaitis R, Wingfield MJ, Wingfield BD (2008) Characterization of the system governing sexual and self-recognition in the white rot homobasidiomycete Amylostereum areolatum. Curr Genet 53:323–336
van der Nest MA, Slippers B, Steenkamp ET, De Vos L, Van Zyl K, Stenlid J, Wingfield MJ, Wingfield BD (2009) Genetic linkage map for Amylostereum areolatum reveals an association betveen vegetative growth and sexual and self-recognition. Fungal Genet Biol 46:632–641
Viviani MA, Esposto MC, Cogliati M, Montagna MT, Wickes BL (2001) Isolation of a Cryptococcus neoformans serotype A MATa strain from the Italian environment. Med Mycol 39:383–386
Viviani MA, Cogliati M, Esposto MC, Lemmer K, Tintelnot K, Valiente MFC, Swinne D, Velegraki A, Velho R (2006) Molecular analysis of 311 Cryptococcus neoformans isolates from a 30-month ECMM survey of cryptococcosis in Europe. FEMS Yeast Res 6:614–619
Votintserva AA, Filatov DA (2009) Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182:1391–1396
Wahl R, Zahiri A, Kämper J (2010) The Ustilago b mating type locus controls hyphal proliferation and expression of secreted virulence factors in planta. Mol Microbiol 75:208–220
Wang P, Perfect JR, Heitman J (2000) G-protein β subunit Gpb1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol Cell Biol 20:352–362
Wang P, Nichols CB, Lengeler KB, Cardenas ME, Cox GM, Perfect PR, Heitman J (2002) Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot Cell 1:257–272
Wendland J, Vaillancourt LJ, Hegner J, Lengeler KB, Laddison KJ, Specht CA, Raper CA, Kothe E (1995) The mating type locus Bβ1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J 14:5271–5278
Whitehouse HLK (1949) Multiple allelomorph heterothallism in fungi. New Phytol 48:212–244
Whitehouse HLK (1952) A survey of heterothallism in the Ustilaginales. Trans Br Mycol Soc 340–355
Wickes BL, Mayorga ME, Edman U, Edman JC (1996) Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the α-mating type. Proc Natl Acad Sci USA 93:7327–7331
Wickes BL, Edman U, Edman JC (1997) The Cryptococcus neoformans STE12α gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol Microbiol 26:951–960
Wong GJ, Wells K (1987) Comparative morphology, compatibility, and interfertility of Auricularia cornea, A. polytricha, and A. tenuis. Mycologia 79:847–858
Wright S, Finnegan D (2001) Genome evolution: sex and the transposable element. Curr Biol 11:R296–R299
Wu C, Huang Y, Yinbing B (2004) RAPD/BSA analysis on monokaryotic strains of different mating types of Auricularia auricula. J Huazhoung Agric Univ, DOI: CNKI:SUN:HZNY.0.2004-01-030
Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramee EE, Kronstad JW, DeAngelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears, R, Yuan B, Dawson TL (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735
Xue CY, Hsueh Y-P, Heitman J (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular fungi. FEMS Microbiol Rev 32:1010–1032
Yamazaki S, Katsuya K (1988) Mating type of pine gall rust fungus, Cronartium quercum. Proc Jpn Acad Ser B 64:197–200
Yan Z, Li XG, Xu JP (2002) Geographic distributions of mating type alleles of Cryptococcus neoformans in four areas of the United States. J Clin Microbiol 40:965–972
Yee AR, Kronstad JW (1998) Dual sets of chimeric alleles identify specificity sequences for the bE and bW mating and pathogenicity genes of Ustilago maydis. Mol Cell Biol 18:221–232
Yi R, Tachikawa T, Ishikawa M, Mukaiyama H, Bao D, Aimi T (2009) Genomic structure of the A mating-type locus in a bipolar basidiomycete, Pholiota nameko. Mycol Res 113:240–248
Yi R, Mukaiyama H, Tachikawa T, Shimomura N, Aimi T (2010) A-mating type gene expression can drive clamp cell formation in the bipolar mushroom Pholiota microspora (Pholiota nameko). Eukaryot Cell 9:1109–1119
Yockteng R, Marthey S, Chiapello HJ, Gendrault A, Hood ME, Rodolphe F, Devier B, Wincker P, Dossat C, Giraud T (2007) Expressed sequences tags of the anther smut fungus, Microbotryum violaceum, identfy mating and pathogenicity genes. BMC Genomics 8:272
Yu Z, Liang J, Cao Z, Guo Z, Dan J, Zhao G (2009) Nuclear behaviour in the life cycle of Melampsora larici-populina Kleb. J Food Agric Env 7:791–794
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 the Y-Z protein binding. Genetics 145:253–260
Yue CL, Cavallo LM, Alspaugh JA, Wang P, Cox GM, Perfect JR, Heitman J (1999) The STE12α homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 153:1601–1615
Zarnack K, Eichhorn H, Kahmann R, Feldbrügge M (2008) Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol 69:1041–1053
Zakharov IA (2005) Intratetrad mating and its genetic and evolutionary consequences. Russian J Genet 41:402–411
Zhao X, Mehrabi R, Xu J (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6:1701–1714
Acknowledgements
Marco A. Coelho is gratefully acknowledged for providing data on Sporidiobolales prior to publication and Marianna Feretzaki for generating Fig. 6.10. The JGI and the Broad-Institute and their staff are thanked for providing genome sequences of various basidiomycetes to the public and all colleagues in the genome annotation teams for any input in definition of mating type genes. This effort was supported in part by R01 grants AI39115 and AI50113 from the NIH/NIAID to J.H.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Kües, U., James, T.Y., Heitman, J. (2011). 6 Mating Type in Basidiomycetes: Unipolar, Bipolar, and Tetrapolar Patterns of Sexuality. In: Pöggeler, S., Wöstemeyer, J. (eds) Evolution of Fungi and Fungal-Like Organisms. The Mycota, vol 14. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19974-5_6
Download citation
DOI: https://doi.org/10.1007/978-3-642-19974-5_6
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-19973-8
Online ISBN: 978-3-642-19974-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)