Skip to main content
Log in

Sexual Reproduction in Dermatophytes

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Sexual reproduction is a rich source of genetic variation and commonly observed among fungi. Basically two different modes of sexual reproduction are observed in fungi, namely heterothallism where two compatible mating types are required to undergo mating and homothallism in which the organism is self-fertile. The genomic region governing the process of sexual reproduction and sex determination is called the mating type (MAT) locus. In filamentous ascomycetes including dermatophytes, the MAT locus harbors two different transcription factor genes in two different mating types. This review focuses on sexual reproduction and the structure of the MAT locus in dermatophytes. The reproductive modes and the observed mating types are summarized for different phylogenetic clades of dermatophytes. In addition, the question of whether or not unisexual reproduction, an interesting form of homothallism, may be the sexual reproduction mode especially in anthropophilic dermatophytes is raised.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Heitman J, Sun S, James TY. Evolution of fungal sexual reproduction. Mycologia. 2013;105:1–27.

    Article  CAS  PubMed  Google Scholar 

  2. Heitman J. Evolution of sexual reproduction: a view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol Rev. 2015;29:108–17.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Fraser JA, Heitman J. Fungal mating-type loci. Curr Biol. 2003;13:R792–5.

    Article  CAS  PubMed  Google Scholar 

  4. Turgeon BG, Yoder OG. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol. 2000;31:1–5.

    Article  CAS  PubMed  Google Scholar 

  5. Butler G. The evolution of MAT: the ascomycetes. In: Heitman J, Kronstad JW, Taylor J, Casselton L, editors. Sex in fungi: molecular determination and evolutionary implications. Washington, DC: ASM Press; 2007. p. 3–18.

    Chapter  Google Scholar 

  6. O’Gorman CM, Fuller H, Dyer PS. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature. 2009;457:471–4.

    Article  PubMed  Google Scholar 

  7. Gioti A, Mushegian AA, Strandberg R, Stajich JE, Johannesson H. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol Biol Evol. 2012;29:3215–26.

    Article  CAS  PubMed  Google Scholar 

  8. Coppin E, Debuchy R, Arnaise S, Picard M. Mating types and sexual development in filamentous ascomycetes. Microbiol Mol Biol Rev. 1997;61:411–28.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Yun SH, Arie T, Kaneko I, Yoder OC, Turgeon BG. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol. 2000;31:7–20.

    Article  CAS  PubMed  Google Scholar 

  10. Yun SH, Berbee ML, Yoder OC, Turgeon BG. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc Natl Acad Sci USA. 1999;96:5592–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Paoletti M, Seymour FA, Alcocer MJ, et al. Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol. 2007;17:1384–9.

    Article  CAS  PubMed  Google Scholar 

  12. Rydholm C, Dyer PS, Lutzoni F. DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell. 2007;6:868–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lin X, Heitman J. Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Sex in fungi: molecular determination and evolutionary implications. Washington, DC: ASM Press; 2007. p. 35–57.

    Chapter  Google Scholar 

  14. Raju NB. Functional heterothallism resulting from homokaryotic conidia and ascospores in Neurospora tetrasperma. Mycol Res. 1992;96:103–16.

    Article  Google Scholar 

  15. Raju NB, Perkins DD. Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Dev Genet. 1994;15:104–18.

    Article  CAS  PubMed  Google Scholar 

  16. Haber JE. Mating-type gene switching in Saccharomyces cerevisiae. Annu Rev Genet. 1998;32:561–99.

    Article  CAS  PubMed  Google Scholar 

  17. Arcangioli B, de Lahondès R. Fission yeast switches mating type by a replication-recombination coupled process. EMBO J. 2000;19:1389–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Feretzaki M, Heitman J. Unisexual reproduction drives evolution of eukaryotic microbial pathogens. PLoS Pathog. 2013;9:e1003674.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kwon-Chung KJ. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia. 1976;68:821–33.

    Article  CAS  PubMed  Google Scholar 

  20. Kwon-Chung KJ, Bennett JE. Distribution of α and α mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol. 1978;108:337–40.

    CAS  PubMed  Google Scholar 

  21. Sun S, Billmyre RB, Mieczkowski PA, Heitman J. Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans. PLoS Genet. 2014;10:e1004849.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lin X, Hull CM, Heitman J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature. 2005;434:1017–21.

    Article  CAS  PubMed  Google Scholar 

  23. Tscharke RL, Lazera M, Chang YC, Wickes BL, Kwon-Chung KJ. Haploid fruiting in Cryptococcus neoformans is not mating type alpha-specific. Fungal Genet Biol. 2003;39:230–7.

    Article  CAS  PubMed  Google Scholar 

  24. Lin X, Litvintseva AP, Nielsen K, et al. αADα hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet. 2007;3:e186.

    Article  PubMed Central  Google Scholar 

  25. Lin X, Patel S, Litvintseva AP, et al. Diploids in the Cryptococcus neoformans serotype A population homozygous for the α mating type originate via unisexual mating. PLoS Pathog. 2009;5:e1000283.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fraser JA, Giles SS, Wenink EC, et al. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature. 2005;437:1360–4.

    Article  CAS  PubMed  Google Scholar 

  27. Bui T, Lin X, Malik R, Heitman J, Carter D. Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, alpha mating type populations. Eukaryot Cell. 2008;7:1771–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Saul N, Krockenberger M, Carter D. Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell. 2008;7:727–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hiremath SS, Chowdhary A, Kowshik T, et al. Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology. 2008;154:1513–24.

    Article  CAS  PubMed  Google Scholar 

  30. Chowdhary A, Hiremath SS, Sun S, et al. Genetic differentiation, recombination and clonal expansion in environmental populations of Cryptococcus gattii in India. Environ Microbiol. 2011;13:1875–88.

    Article  CAS  PubMed  Google Scholar 

  31. Alby K, Schaefer D, Bennett RJ. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature. 2009;460:890–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Mahoney DP, Huang LH, Backus MP. New homothallic Neurosporas from tropical soils. Mycologia. 1969;61:264–72.

    Article  CAS  PubMed  Google Scholar 

  33. Nygren K, Strandberg R, Wallberg A, et al. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol Phylogenet Evol. 2011;59:649–63.

    Article  PubMed  Google Scholar 

  34. Glass NL, Vollmer SJ, Staben C, et al. DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science. 1988;241:570–3.

    Article  CAS  PubMed  Google Scholar 

  35. Glass NL, Smith ML. Structure and function of a mating-type gene from the homothallic species Neurospora africana. Mol Gen Genet. 1994;244:401–9.

    Article  CAS  PubMed  Google Scholar 

  36. Arnaise S, Zickler D, Glass NL. Heterologous expression of mating-type genes in filamentous fungi. Proc Natl Acad Sci USA. 1993;90:6616–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Inderbitzin P, Harkness J, Turgeon BG, Berbee ML. Lateral transfer of mating system in Stemphylium. Proc Natl Acad Sci USA. 2005;102:11390–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Wilson AM, Godlonton T, van der Nest MA, et al. Unisexual reproduction in Huntiella moniliformis. Fungal Genet Biol. 2015;80:1–9.

    Article  CAS  PubMed  Google Scholar 

  39. White TC, Oliver BG, Gräser Y, Henn MR. Generating and testing molecular hypotheses in the dermatophytes. Eukaryot Cell. 2008;7:1238–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Summerbell RC. Form and function in the evolution of dermatophytes. In: Kushwaha RKS, Guarro J, editors. Biology of Dermatophytes and other Keratinophilic Fungi. Bilbao: Revista Iberoamericana de Micología; 2000. p. 30–43.

    Google Scholar 

  41. Hull CM, Raisner RM, Johnson AD. Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science. 2000;289:307–10.

    Article  CAS  PubMed  Google Scholar 

  42. Stockdale PM. Sexual stimulation between Arthroderma simii Stockd., Mackenzie & Austwick and related species. Sabouraudia. 1968;6:176–81.

    Article  CAS  PubMed  Google Scholar 

  43. Gräser Y, Scott J, Summerbell R. The new species concept in dermatophytes—a polyphasic approach. Mycopathologia. 2008;166:239–56.

    Article  PubMed  Google Scholar 

  44. Woodgyer A. The curious adventures of Trichophyton equinum in the realm of molecular biology: a modern fairy tale. Med Mycol. 2004;42:397–403.

    Article  CAS  PubMed  Google Scholar 

  45. Summerbell RC. What is the evolutionary and taxonomic status of asexual lineages in the dermatophytes? Stud Mycol. 2002;47:97–101.

    Google Scholar 

  46. Li W, Metin B, White TC, Heitman J. Organization and evolutionary trajectory of the mating type (MAT) locus in dermatophyte and dimorphic fungal pathogens. Eukaryot Cell. 2010;9:46–58.

    Article  CAS  PubMed  Google Scholar 

  47. Burmester A, Shelest E, Glöckner G, et al. Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol. 2011;12:R7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fraser JA, Stajich JE, Tarcha EJ, et al. Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. Eukaryot Cell. 2007;6:622–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cafarchia C, Iatta R, Latrofa MS, Gräser Y, Otranto D. Molecular epidemiology, phylogeny and evolution of dermatophytes. Infect Genet Evol. 2013;20:336–51.

    Article  PubMed  Google Scholar 

  50. Takashio M. Une nouvelle forme sexuée du complexe Trichophyton mentagrophytes, Arthroderma vanbreuseghemii sp. nov. Ann Parasitol Hum Comp. 1973;48:713–32.

    Google Scholar 

  51. Symoens F, Jousson O, Planard C, et al. Molecular analysis and mating behaviour of the Trichophyton mentagrophytes species complex. Int J Med Microbiol. 2011;301:260–6.

    Article  CAS  PubMed  Google Scholar 

  52. Kano R, Kawasaki M, Mochizuki T, Hiruma M, Hasegawa A. Mating genes of the Trichophyton mentagrophytes complex. Mycopathologia. 2012;173:103–12.

    Article  CAS  PubMed  Google Scholar 

  53. Martinez DA, Oliver BG, Gräser Y, et al. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. mBio. 2012;3:e00259–12.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Hiruma J, Okubo M, Kano R, et al. Mating type gene (MAT) and itraconazole susceptibility of Trichophyton tonsurans strains isolated in Japan. Mycopathologia. 2016;181:441–4.

    Article  CAS  PubMed  Google Scholar 

  55. Stockdale PM, Mackenzie DWR. Austwick PKC. Arthroderma simii sp. nov., the perfect state of Trichophyton simii (Pinoy) comb. nov. Sabouraudia. 1965;4:112–23.

    Article  CAS  PubMed  Google Scholar 

  56. Ajello L, Cheng S. The perfect state of Trichophyton mentagrophytes. Sabouraudia. 1967;5:230–4.

    Article  CAS  PubMed  Google Scholar 

  57. Takashio M. Is Arthroderma benhamiae the perfect state of Trichophyton mentagrophytes? Sabouraudia. 1972;10:122–7.

    Article  CAS  PubMed  Google Scholar 

  58. Symoens F, Jousson O, Packeu A, et al. The dermatophyte species Arthroderma benhamiae: intraspecies variability and mating behaviour. J Med Microbiol. 2013;62:377–85.

    Article  CAS  PubMed  Google Scholar 

  59. Kano R, Yamada T, Makimura K, et al. Arthroderma benhamiae (the teleomorph of Trichophyton mentagrophytes) mating type-specific genes. Mycopathologia. 2011;171:333–7.

    Article  CAS  PubMed  Google Scholar 

  60. Kano R, Yoshida E, Yaguchi T, et al. Mating type gene (MAT1-2) of Trichophyton verrucosum. Mycopathologia. 2014;177:87–90.

    Article  CAS  PubMed  Google Scholar 

  61. Gräser Y, De Hoog S, Summerbell RC. Dermatophytes: recognizing species of clonal fungi. Med Mycol. 2006;44:199–209.

    Article  PubMed  Google Scholar 

  62. Kano R, Isizuka M, Hiruma M, et al. Mating type gene (MAT1-1) in Japanese isolates of Trichophyton rubrum. Mycopathologia. 2013;175:171–3.

    Article  CAS  PubMed  Google Scholar 

  63. Anzawa K, Kawasaki M, Mochizuki T, Ishizaki H. Successful mating of Trichophyton rubrum with Arthroderma simii. Med Mycol. 2010;48:629–34.

    Article  CAS  PubMed  Google Scholar 

  64. Sequeira H, Cabrita J, De Vroey C, Wuytack-Raes C. Contribution to our knowledge of Trichophyton megninii. J Med Vet Mycol. 1991;29:417–8.

    Article  CAS  PubMed  Google Scholar 

  65. Stockdale PM. Nannizzia incurvata gen. nov., sp. nov., a perfect state of Microsporum gypseum (Bodin) Guiart et Grigorakis. Sabouraudia. 1961;1:41–8.

    Article  Google Scholar 

  66. Stockdale PM. The Microsporum gypseum complex (Nannizzia incurvata Stockd., N. gypsea (Nann.) comb. nov., N. fulva sp. nov.). Sabouraudia. 1963;3:114–26.

    Article  CAS  PubMed  Google Scholar 

  67. Weitzman I, Silva-Hutner M. Non-keratinous agar media as substrates for the ascigerous state in certain members of the Gymnoascaceae pathogenic for man and animals. Sabouraudia. 1967;5:335–40.

    Article  CAS  PubMed  Google Scholar 

  68. Weitzman I. Incompatibility in the Microsporum gypseum complex. Mycologia. 1964;56:425–35.

    Article  Google Scholar 

  69. Dawson CO, Gentles JC. The perfect states of Keratinomyces ajelloi Vanbreuseghem, Trichophyton terrestre Durie & Frey and Microsporum nanum Fuentes. Sabouraudia. 1961;1:49–57.

    Article  CAS  PubMed  Google Scholar 

  70. Weitzman I, McGinnis MR, Padhye AA, Ajello L. The genus Arthroderma and its later synonym Nannizzia. Mycotaxon. 1986;25:505–18.

    Google Scholar 

  71. Stockdale PM. Nannizzia persicolor sp. nov., the perfect state of Trichophyton persicolor Sabouraud. Sabouraudia. 1967;5:355–9.

    Article  CAS  PubMed  Google Scholar 

  72. Takashio M. Mating behaviour of Nannizzia corniculata. Mycotaxon. 1982;14:375–82.

    Google Scholar 

  73. Takashio M, De Vroey D. Nannizzia corniculata sp. nov., the perfect state of Microsporum boullardii. Mycotaxon. 1982;14:383–9.

    Google Scholar 

  74. Kaszubiak A, Klein S, de Hoog GS, Gräser Y. Population structure and evolutionary origins of Microsporum canis, M. ferrugineum and M. audouinii. Infect Genet Evol. 2004;4:179–86.

    Article  CAS  PubMed  Google Scholar 

  75. Sharma R, de Hoog S, Presber W, Gräser Y. A virulent genotype of Microsporum canis is responsible for the majority of human infections. J Med Microbiol. 2007;56:1377–85.

    Article  CAS  PubMed  Google Scholar 

  76. Ajello L. The ascigerous state of Microsporum cookei. Sabouraudia. 1961;1:173–7.

    Article  CAS  PubMed  Google Scholar 

  77. De Clercq D. Nannizzia cookiella, a new species of dermatophyte. Mycotaxon. 1983;18:23–8.

    Google Scholar 

  78. Georg LK, Ajello L, Friedman L, Brinkman SA. A new species of Microsporum pathogenic to man and animals. Sabouraudia. 1962;1:189–96.

    Article  CAS  PubMed  Google Scholar 

  79. Rush-Munro FM, Smith JMB, Borelli D. The perfect state of Microsporum racemosum. Mycologia. 1970;62:856–9.

    Article  CAS  PubMed  Google Scholar 

  80. Choi JS, Gräser Y, Walther G, et al. Microsporum mirabile and its teleomorph Arthroderma mirabile, a new dermatophyte species in the M. cookei clade. Med Mycol. 2012;50:161–9.

    Article  PubMed  Google Scholar 

  81. Howard DH, Weitzman I, Padhye AA. Onygenales: Arthrodermataceae. In: Howard DH, editor. Pathogenic Fungi in Humans and Animals. NewYork, NY: Marcel Dekker Inc; 2003. p. 141–95.

    Google Scholar 

  82. Ajello L, Cheng SL. A new geophilic Trichophyton. Mycologia. 1967;59:255–63.

    Article  Google Scholar 

  83. Böhme H. Arthroderma gertleri sp. nov., the perfect form of Trichophyton vanbreuseghemii Rioux, Jarry et Juminer. Mycoses. 1967;10:247–52.

    Article  Google Scholar 

  84. Pore RS, Tsao GC, Plunkett OA. A new species of Arthroderma established according to biological species concepts. Mycologia. 1965;57:969–73.

    Article  Google Scholar 

  85. Padhye AA, Carmichael JW. Arthroderma insingulare sp. nov., another gymnoascaceous state of the Trichophyton terrestre complex. Sabouraudia. 1972;10:47–51.

    Article  CAS  PubMed  Google Scholar 

  86. Dawson CO. Two new species of Arthroderma isolated from soil from rabbit burrows. Sabouraudia. 1963;2:185–91.

    Article  Google Scholar 

  87. Rees RG. Arthroderma flavescens sp. nov. Sabouraudia. 1967;5:206–8.

    Article  CAS  PubMed  Google Scholar 

  88. Krivanec K, Janecková V, Otcenásek M. Arthroderma melis spec. nov.—a new dermatophyte species isolated from badger burrows in Czechoslovakia. Ceská Mykologie. 1977;31:91–9.

    Google Scholar 

  89. Varsavsky E, Ajello L. The perfect and imperfect forms of a new keratinophilic fungus: Arthroderma ciferrii sp. nov.: Trichophyton georgii sp. nov. Riv Patol Veg. 1964;4:351–64.

    Google Scholar 

  90. Udagawa SI. Geographical distribution of the pleomorphic plectomycetes in Asia and their teleomorph-anamorph connections. In: Sugiyama J (ed) Pleomorphic fungi: the diversity and its taxonomic implications. Kodansha LTD, Tokyo and Elsevier Science Publishers B. V., Amsterdam, 1987, pp. 9–28.

  91. Sekhon AS, Padhye AA, Carmichael JW. Mating reactions in Arthroderma tuberculatum. Sabouraudia. 1973;11:283–6.

    Article  CAS  PubMed  Google Scholar 

  92. Campbell CK, Borman AM, Linton CJ, Bridge PD, Johnson EM. Arthroderma olidum, sp. nov. A new addition to the Trichophyton terrestre complex. Med Mycol. 2006;44:451–9.

    Article  PubMed  Google Scholar 

  93. Varsavsky E, Reca ME. Demonstration of heterothallism in Ctenomyces serratus Eidam 1880. Mycopathol Mycol Appl. 1964;24:119–20.

    Article  CAS  PubMed  Google Scholar 

  94. Orr GF, Kuehn HH. The genus Ctenomyces Eidam. Mycopathol Mycol Appl. 1963;21:321–33.

    Article  CAS  PubMed  Google Scholar 

  95. Moraes M, Padhye AA, Ajello L. The perfect state of Microsporum amazonicum. Mycologia. 1975;67:1109–13.

    Article  CAS  PubMed  Google Scholar 

  96. Hubka V, Cmokova A, Skorepova M, Mikula P, Kolarik M. Trichophyton onychocola sp. nov. isolated from human nail. Med Mycol. 2014;52:285–92.

    Article  CAS  PubMed  Google Scholar 

  97. Hubka V, Nissen CV, Jensen RH, et al. Discovery of a sexual stage in Trichophyton onychocola, a presumed geophilic dermatophyte isolated from toenails of patients with a history of T. rubrum onychomycosis. Med Mycol. 2015;53:798–809.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Banu Metin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Metin, B., Heitman, J. Sexual Reproduction in Dermatophytes. Mycopathologia 182, 45–55 (2017). https://doi.org/10.1007/s11046-016-0072-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-016-0072-x

Keywords

Navigation