Abstract
The capability of sexual reproduction is distributed across the eukaryotes, including the fungi. A primary influence in the sexual interaction is the exchange of information mediated by diffusible molecules, called sexual pheromones. This chapter examines the biosynthesis of pheromones and the sexual responses induced by them in different branches of the fungal kingdom, with an emphasis on the early lineages. The best-studied species are members of the Dikarya and they use pheromones derived from peptide precursors. In contrast, members of the Mucoromycotina use apocarotenoids while the Blastocladiomycota use sesquiterpenes. Comparison between these pheromones establishes evolutionary trends among the fungal lineages.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
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 9:3491–3498
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 263:18236–18240
Aragón CMG, Murillo FJ, De La Guardia MD, Cerdá-Olmedo E (1976) An enzyme complex for the dehydrogenation of phytoene in Phycomyces. Eur J Biochem 63:71–75
Arrach N, Fernández-Martín R, Cerdá-Olmedo E, Avalos J (2001) A single gene for lycopene cyclase, phytoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc Natl Acad Sci USA 98:1687–1692
Bakkeren G, Kronstad JW (1994) Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci USA 91:7085–7089
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
Bardwell L (2005) A walk-through of the yeast mating pheromone response pathway. Peptides 26:339–350
Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. Croom Helm, London
Betz R, Crabb JW, Meyer HE, Wittig R, Duntze W (1987) Amino acid sequences of a-factor mating peptides from Saccharomyces cerevisiae. J Biol Chem 262:546–548
Blackwell M (2011) The fungi: 1, 2, 3 … 5.1 million species? Am J Bot 98:426–438
Blakeslee AF (1904) Sexual reproduction in the Mucorineae. Proc Am Acad Arts Sci 40:205–319
Bölker M, Kahmann R (1993) Sexual pheromones and mating responses in fungi. Plant Cell 5:1461–1469
Bu’Lock JD, Jones BE, Winskill N (1976) The apocarotenoid system of sex hormones and prohormones in Mucorales. Pure Appl Chem 47:191–202
Burgeff H (1924) Untersuchungen über Sexualität und Parasitismus bei Mucorineen. Bot Abh 4:1–135
Burmester A, Richter A, Schultze K, Voelz K, Schachtschabel D, Boland W, Wöstemeyer J, Schimek C (2007) Cleavage of β-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase. Fungal Genet Biol 44:1096–1108
Butenandt A, Beckamnn R, Hecker E (1961) On the sex attractant of silk-moths. I. The biological test and the isolation of the pure sex-attractant bombykol. Hoppe Seylers Z Physiol Chem 324:71–83
Caglioti L, Cainelli G, Camerino B, Mondelli R, Prieto A, Quilico A, Salvatori T, Selva A (1966) The structure of trisporic-C acid. Tetrahedron 22(Suppl):175–187
Cainelli G, Grasselli P, Selva A (1967) Struttura dell’acido trisporico B. La Chimica e L’Industria 49:628–629
Caldwell GA, Naider F, Becker JM (1995) Fungal lipopeptide mating pheromones: a model system for protein prenylation. Microbiol Rev 59:406–422
Casselton LA (2008) Fungal sex genes-searching for the ancestors. Bioessays 30:711–714
Casselton LA, Olesnicky NS (1998) Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62:55–70
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
Coelho MA, Rosa A, Rodrigues N, Fonseca A, Gonçalves 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 7:1053–1061
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
Coppin E, de Renty C, Debuchy R (2005) The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryot Cell 4:407–420
Czempinski K, Kruft V, Wöstemeyer J, Burmester A (1996) 4-dihydromethyltrisporate dehydrogenase from Mucor mucedo, an enzyme of the sexual hormone pathway: purification, and cloning of the corresponding gene. Microbiology 142:2647–2654
Drinkard LC, Nelson GE, Sutter RP (1982) Growth arrest: a prerequisite for sexual development in Phycomyces blakesleeanus. Exp Mycol 6:52–59
Dyer PS (2008) Evolutionary biology: genomic clues to original sex in fungi. Curr Biol 18:207–209
Eslava AP, Cerdá-Olmedo E (1974) Genetic control of phytoene dehydrogenation in Phycomyces. Plant Sci Lett 2:9–14
Findley K, Sun S, Fraser JA, Hsueh YP, Averette AF, Li W, Dietrich FS, Heitman J (2012) Discovery of a modified tetrapolar sexual cycle in Cryptococcus amylolentus and the evolution of MAT in the Cryptococcus species complex. PLoS Genet 8:e1002528
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, 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
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:e384
García-Muse T, Steinberg G, Pérez-Martín J (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell 2:494–500
Gola S, Kothe E (2003) The little difference: in vivo analysis of pheromone discrimination in Schizophyllum commune. Curr Genet 42:276–283
Gooday GW, Adams DJ (1993) Sex hormones and fungi. Adv Microb Physiol 34:69–145
Gryganskyi 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:e15273
Haber JE (1998) Mating-type gene switching in Saccharomyces cerevisiae. Annu Rev Genet 32:561–599
Heisenberg M, Cerdá-Olmedo E (1968) Segregation of heterokaryons in the asexual cycle of Phycomyces. Mol Gen Genet 102:187–195
Heitman J (2010) Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8:86–99
Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) (2007) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC
Herskowitz I (1988) Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev 52:536–553
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Thorsten Lumbsch H, 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 Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux 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 Y-J, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547
Hsueh YP, Heitman J (2008) Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr Opin Microbiol 11:517–524
Idnurm A, Walton FJ, Floyd A, Heitman J (2008) Identification of the sex genes in an early diverged fungus. Nature 451:193–197
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
Jones SK Jr, Bennett RJ (2011) Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48:668–676
Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, Richards TA (2011) Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474:200–203
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 Comun 83:1077–1083
Karlson P, Lüsher M (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183:55–56
Kellner M, Burmester A, Wöstemeyer A, Wöstemeyer J (1993) Transfer of genetic information from the mycoparasite Parasitella parasitica to its host Absidia glauca. Curr Genet 23:334–337
Kothe E (2008) Sexual attraction: on the role of fungal pheromone/receptor systems. Acta Microbiol Immunol Hung 55:125–143
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, Byrnes EJ, Torres-Martinez S, Dietrich FS, Keeling PJ, Heitman J (2008) Microsporidia evolved from ancestral sexual fungi. Curr Biol 18:1675–1679
Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74:298–340
Lengeler KB, Davidson RC, D’Souza C, Harashima T, Shen W-C, Wang P, Pan X, Waugh M, Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785
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 CH, Cervantes M, Springer DJ, Boekhout T, Ruiz-Vazquez RM, Torres-Martinez SR, Heitman J, Lee SC (2011) Sporangiospore size dimorphism is linked to virulence of Mucor circinelloides. PLoS Pathog 7:e1002086
Machlis L (1968) The response of wild type male gametes of Allomyces to sirenin. Plant Physiol 43:1319–1320
Madhani H (2007) From a to α: yeast as a model for cellular differentiation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET (2011) Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Mol Biol Evol 28:1987–2003
Maynard Smith J (1970) Natural selection and the concept of a protein space. Nature 225:563–564
Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge
Medina HR, Cerdá-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82:199–208
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
Michaelis S, Herskowitz I (1988) The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol Cell Biol 8:1309–1318
Miller ML, Sutter RP (1984) Methyl trisporate E. A sex pheromone in Phycomyces blakesleeanus? J Biol Chem 259:6420–6422
Morrow CA, Fraser JA (2009) Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res 9:161–177
Naider F, Becker JM (2004) The α-factor mating pheromone of Saccharomyces cerevisiae: a model for studying the interaction of peptide hormones and G protein-coupled receptors. Peptides 25:1441–1463
Nielsen K, Heitman J (2007) Sex and virulence of human pathogenic fungi. Adv Genet 57:143–173
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
Pöggeler S (2001) Mating-type genes for classical strain improvements of ascomycetes. Appl Microbiol Biotechnol 56:589–601
Polaino S, Gonzalez-Delgado JA, Arteaga P, Herrador MM, Barrero AF, Cerdá-Olmedo E (2012) Apocarotenoids in the sexual interaction of Phycomyces blakesleeanus. Org Biomol Chem 10:3002–3009
Polaino S, Herrador M, Cerdá-Olmedo E, Barrero AF (2010) Splitting of β-carotene in the sexual interaction of Phycomyces. Org Biomol Chem 8:4229–4231
Pommerville J, Olson LW (1987) Evidence for a male-produced pheromone in Allomyces macrogynus. Exp Mycol 11:245–248
Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9:847–859
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
Schachtschabel D, David A, Menzel K-D, Schimek C, Wöstemeyer J, Boland W (2008) Cooperative biosynthesis of trisporoids by the (+) and (−) mating types of the zygomycete Blakeslea trispora. ChemBioChem 15:3004–3012
Schimek C, Wöstemeyer J (2009) Carotene derivatives in sexual communication of zygomycete fungi. Phytochemistry 70:1867–1875
Schimek C, Kleppe K, Saleem AR, Voigt K, Burmester A, Wöstemeyer J (2003) Sexual reactions in Mortierellales are mediated by the trisporic acid system. Mycol Res 107:736–747
Schmoll M, Seibel C, Tisch D, Dorrer M, Kubicek CP (2010) A novel class of peptide pheromone precursors in ascomycetous fungi. Mol Microbiol 77:1483–1501
Schultze K, Schimek C, Wöstemeyer J, Burmester A (2005) Sexuality and parasitism share common regulatory pathways in the fungus Parasitella parasitica. Gene 348:33–44
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
Spalla C (1963) Ricerche sulla riproduzione sessuale in Mucorales. Studio della riproduzione sessuale in Phycomyces blakesleeanus e in Choanephora circinans e comparazione con quella di Cunninghamella blakesleeana, C. elegans, Mucor hiemalis e M. racemosus. Riv Patol Veg 3:189–198
Sprague GF, Thorner JW (1992) Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae. In: Broach JR, Pringle JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces: gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 657–744
Stanton BC, Giles SS, Staudt MW, Kruzel EK, Hull CM (2010) Allelic exchange of pheromones and their receptors reprograms sexual identity in Cryptococcus neoformans. PLoS Genet 6:e1000860
Sutter RP (1970) Trisporic acid synthesis in Blakeslea trispora. Science 168:1590–1592
Sutter RP (1986) Apotrisporin-E: a new sesquiterpenoid isolated from Phycomyces blakesleeanus and Blakeslea trispora. Exp Mycol 10:256–258
Sutter RP (1987) Sexual development. In: Cerdá-Olmedo E, Lipson ED (eds) Phycomyces. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 317–336
Sutter RP, Whitaker JP (1981) Zygophore-stimulating precursors (pheromones) of trisporic acids active in (−)-Phycomyces blakesleeanus. Acid-catalyzed anhydro derivates of methyl 4-dihydrotrisporate-C and 4-dihydrotrisporate-C. J Biol Chem 256:2334–2341
Sutter RP, Zawodny PD (1984) Apotrisporin: a major metabolite of Blakeslea trispora. Exp Mycol 8:89–92
Sutter RP, Capage DA, Harrison TL, Keen WA (1973) Trisporic acid biosynthesis in separate plus and minus cultures of Blakeslea trispora: Identification by Mucor assay of two mating-type-specific components. J Bacteriol 114:1074–1082
Sutter RP, Harrison TL, Galasko G (1974) Trisporic acid biosynthesis in Blakeslea trispora via mating type-specific precursors. J Biol Chem 249:2282–2284
Tagua V, Medina HR, Martín-Domínguez R, Eslava AP, Corrochano LM, Cerdá-Olmedo E, Idnurm A (2012) A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus. Fungal Genet Biol 49. doi:10.1016/j.fgb.2012.03.002
Torres-Martínez S, Murillo FJ, Cerdá-Olmedo E (1980) Genetics of lycopene cyclization and substrate transfer in β-carotene biosynthesis in Phycomyces. Genet Res 36:299–309
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
van den Ende H (1968) Relationship between sexuality and carotene synthesis in Blakeslea trispora. J Bacteriol 96:1298–1303
van Peer AF, Park S-Y, Shin P-G, Jang K-Y, Yoo Y-B, Park Y-P, Lee B-M, Sung G-H, James TY, Kong W-S (2011) Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS One 6:e22249
Von Lintig J, Vogt K (2000) Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving β-carotene to retinal. J Biol Chem 275:11915–11920
Wang L, Chen W, Feng Y, Ren Y, Gu Z, Chen H, Wang H, Thomas MJ, Zhang B, Berquin IM, Li Y, Wu J, Zhang H, Song Y, Liu X, Norris JS, Wang S, Du P, Shen J, Wang N, Yang Y, Wang W, Feng L, Ratledge C, Zhang H, Chen YQ (2011) Genome characterization of the oleaginous fungus Mortierella alpina. PLoS One 6:e28319
Werkman BA (1976) Localization and partial characterization of a sex-specific enzyme in homothallic and heterothallic Mucorales. Arch Microbiol 109:209–213
Werkman BA, van den Ende H (1973) Trisporic acid synthesis in Blakeslea trispora. Arch Microbiol 90:365–374
Wetzel J, Burmester A, Kolbe M, Wöstemeyer J (2012) The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones. Microbiology 158:1016–1023
Wetzel J, Scheibner O, Burmester A, Schimek C, Wöstemeyer J (2009) 4-dihydrotrisporin-dehydrogenase, an enzyme of the sex hormone pathway of Mucor mucedo: purification, cloning of the corresponding gene, and developmental expression. Eukaryot Cell 8:88–95
Williams GC (1975) Sex and evolution. Monogr Popul Biol 8:3–200
Wöstemeyer J, Wöstemeyer A, Burmester A, Czempinski K (1995) Relationships between sexual processes and parasitic interactions in the host-pathogen system Absidia glauca-Parasitella parasitica. Can J Bot 73(Suppl 1):S243–S250
Xue C, Hsueh Y-P, Heitman J (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32:1010–1032
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Polaino, S., Idnurm, A. (2012). Sexual Pheromones in the Fungi. In: Witzany, G. (eds) Biocommunication of Fungi. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4264-2_11
Download citation
DOI: https://doi.org/10.1007/978-94-007-4264-2_11
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-4263-5
Online ISBN: 978-94-007-4264-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)