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Annual Review of Genetics

Volume 53, 2019

The Evolution of Sexual Reproduction and the Mating-Type Locus: Links to Pathogenesis of Human Pathogenic Fungi

Abstract

species utilize a variety of sexual reproduction mechanisms, which generate genetic diversity, purge deleterious mutations, and contribute to their ability to occupy myriad environmental niches and exhibit a range of pathogenic potential. The bisexual and unisexual cycles of pathogenic species are stimulated by properties associated with their environmental niches and proceed through well-characterized signaling pathways and corresponding morphological changes. Genes governing mating are encoded by the mating-type () loci and influence pathogenesis, population dynamics, and lineage divergence in . has undergone significant evolutionary changes within the genus, including transition from the ancestral tetrapolar state in nonpathogenic species to a bipolar mating system in pathogenic species, as well as several internal reconfigurations. Owing to the variety of established sexual reproduction mechanisms and the robust characterization of the evolution of mating and in this genus, species provide key insights into the evolution of sexual reproduction.

Keyword(s): eukaryotic microbial evolution, fungal pathogenesis, MAT locus, mating type, medical mycology, sexual reproduction
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/content/journals/10.1146/annurev-genet-120116-024755
2019-12-03
2024-04-24
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Literature Cited

  1. 1. 
    Alspaugh JA, Perfect JR, Heitman J 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev 11:3206–17
     [Google Scholar]
  2. 2. 
    Alvarez M, Casadevall A. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16:2161–65
     [Google Scholar]
  3. 3. 
    Bakkeren G, Kronstad JW. 1994. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. PNAS 91:7085–89
     [Google Scholar]
  4. 4. 
    Bennett RJ, Turgeon BG. 2017. Fungal sex: the Ascomycota. The Fungal Kingdom J Heitman, BJ Howlett, PW Crous, EH Stukenbrock, TY James, NAR Gow 117–45 Washington, DC: ASM Press
     [Google Scholar]
  5. 5. 
    Berchowitz LE, Copenhaver GP. 2010. Genetic interference: Don't stand so close to me. Curr. Genom. 11:91–102
     [Google Scholar]
  6. 6. 
    Bergero R, Charlesworth D. 2009. The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 24:94–102
     [Google Scholar]
  7. 7. 
    Billmyre RB, Clancey SA, Heitman J 2017. Natural mismatch repair mutations mediate phenotypic diversity and drug resistance in Cryptococcus deuterogattii. eLife 6:e28802
     [Google Scholar]
  8. 8. 
    Billmyre RB, Croll D, Li W, Mieczkowski P, Carter DA et al. 2014. Highly recombinant VGII Cryptococcus gattii population develops clonal outbreak clusters through both sexual macroevolution and asexual microevolution. mBio 5:e01494–14
     [Google Scholar]
  9. 9. 
    Boekhout T, Belkum AV. 1997. Variability of karyotypes and RAPD types in genetically related strains of Cryptococcus neoformans. Curr. Genet 32:203–8
     [Google Scholar]
  10. 10. 
    Botts MR, Giles SS, Gates MA, Kozel TR, Hull CM 2009. Isolation and characterization of Cryptococcus neoformans spores reveal a critical role for capsule biosynthesis genes in spore biogenesis. Eukaryot. Cell 8:595–605
     [Google Scholar]
  11. 11. 
    Branco S, Badouin H, Rodríguez de la Vega RC, Gouzy J, Carpentier F et al. 2017. Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism. PNAS 114:7067–72
     [Google Scholar]
  12. 12. 
    Branco S, Carpentier F, Rodríguez de la Vega RC, Badouin H, Snirc A et al. 2018. Multiple convergent supergene evolution events in mating-type chromosomes. Nat. Commun. 9:2000
     [Google Scholar]
  13. 13. 
    Carpentier F, Rodríguez de la Vega RC, Branco S, Snirc A, Coelho MA et al. 2019. Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi. Genome Res 29:944–53
     [Google Scholar]
  14. 14. 
    Casadevall A. 2012. Amoeba provide insight into the origin of virulence in pathogenic fungi. Adv. Exp. Med. Biol. 710:1–10
     [Google Scholar]
  15. 15. 
    Casadevall A, Freij JB, Hann-Soden C, Taylor J 2017. Continental drift and speciation of the Cryptococcus neoformans and Cryptococcus gattii species complexes. mSphere 2:e00103–17
     [Google Scholar]
  16. 16. 
    Casadevall A, Perfect JR. 1998. Cryptococcus neoformans Washington, DC: ASM Press
  17. 17. 
    Chambers SR, Hunter N, Louis EJ, Borts RH 1996. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16:6110–20
     [Google Scholar]
  18. 18. 
    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. PNAS 98:3258–63
     [Google Scholar]
  19. 19. 
    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. 191:871–82
     [Google Scholar]
  20. 20. 
    Chitty JL, Edwards DJ, Robertson AAB, Butler MS, Duley JA et al. 2019. Quantitation of purines from pigeon guano and implications for Cryptococcus neoformans survival during infection. Mycopathologia 184:273–81
     [Google Scholar]
  21. 21. 
    Chowdhary A, Hiremath SS, Sun S, Kowshik T, Randhawa HS, Xu J 2011. Genetic differentiation, recombination and clonal expansion in environmental populations of Cryptococcus gattii in India. Environ. Microbiol. 13:1875–88
     [Google Scholar]
  22. 22. 
    Chowdhary A, Randhawa HS, Prakash A, Meis JF 2012. Environmental prevalence of Cryptococcus neoformans and Cryptococcus gattii in India: an update. Crit. Rev. Microbiol. 38:1–16
     [Google Scholar]
  23. 23. 
    Coelho MA, Bakkeren G, Sun S, Hood ME, Giraud T 2017. Fungal sex: the Basidiomycota. The Fungal Kingdom J Heitman, BJ Howlett, PW Crous, EH Stukenbrock, TY James, NAR Gow 147–75 Washington, DC: ASM Press
     [Google Scholar]
  24. 24. 
    Coelho MA, Sampaio JP, Gonçalves P 2013. Living and thriving on the skin: Malassezia genomes tell the story. mBio 4:e00117–13
     [Google Scholar]
  25. 25. 
    Crabtree JN, Okagaki LH, Wiesner DL, Strain AK, Nielsen JN, Nielsen K 2012. Titan cell production enhances the virulence of Cryptococcus neoformans. Infect. Immun 80:3776–85
     [Google Scholar]
  26. 26. 
    Dambuza IM, Drake T, Chapuis A, Zhou X, Correia J et al. 2018. The Cryptococcus neoformans titan cell is an inducible and regulated morphotype underlying pathogenesis. PLOS Pathog 14:e1006978
     [Google Scholar]
  27. 27. 
    Davidson RC, Moore TD, Odom AR, Heitman J 2000. Characterization of the MFα pheromone of the human fungal pathogen Cryptococcus neoformans. Mol. Microbiol 38:1017–26
     [Google Scholar]
  28. 28. 
    Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ, Oliver SG 2003. Engineering evolution to study speciation in yeasts. Nature 422:68–72
     [Google Scholar]
  29. 29. 
    Desjardins CA, Giamberardino C, Sykes SM, Yu C-H, Tenor JL et al. 2017. Population genomics and the evolution of virulence in the fungal pathogen Cryptococcus neoformans. Genome Res 27:1207–19
     [Google Scholar]
  30. 30. 
    Dromer F, Varma A, Ronin O, Mathoulin S, Dupont B 1994. Molecular typing of Cryptococcus neoformans serotype D clinical isolates. J. Clin. Microbiol. 32:2364–71
     [Google Scholar]
  31. 31. 
    D'Souza CA, Kronstad JW, Taylor G, Warren R, Yuen M et al. 2011. Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. mBio 2:e00342–10
     [Google Scholar]
  32. 32. 
    Engelthaler DM, Hicks ND, Gillece JD, Roe CC, Schupp JM et al. 2014. Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. mBio 5:e01464–14
     [Google Scholar]
  33. 33. 
    Et-Touil A, Brasier CM, Bernier L 1999. Localization of a pathogenicity gene in Ophiostoma novo-ulmi and evidence that it may be introgressed from O. ulmi. Mol. Plant-Microbe Interact 12:6–15
     [Google Scholar]
  34. 34. 
    Farrer RA, Desjardins CA, Sakthikumar S, Gujja S, Saif S et al. 2015. Genome evolution and innovation across the four major lineages of Cryptococcus gattii. mBio 6:e00868–15
     [Google Scholar]
  35. 35. 
    Feretzaki M, Billmyre RB, Clancey SA, Wang X, Heitman J 2016. Gene network polymorphism illuminates loss and retention of novel RNAi silencing components in the Cryptococcus pathogenic species complex. PLOS Genet 12:e1005868
     [Google Scholar]
  36. 36. 
    Feretzaki M, Hardison SE, Wormley FL Jr., Heitman J 2014. Cryptococcus neoformans hyperfilamentous strain is hypervirulent in a murine model of cryptococcal meningoencephalitis. PLOS ONE 9:e104432
     [Google Scholar]
  37. 37. 
    Feretzaki M, Heitman J. 2013. Genetic circuits that govern bisexual and unisexual reproduction in Cryptococcus neoformans. PLOS Genet 9:e1003688
     [Google Scholar]
  38. 38. 
    Findley K, Rodriguez-Carres M, Metin B, Kroiss J, Fonseca A et al. 2009. Phylogeny and phenotypic characterization of pathogenic Cryptococcus species and closely related saprobic taxa in the Tremellales. Eukaryot. Cell 8:353–61
     [Google Scholar]
  39. 39. 
    Findley K, Sun S, Fraser JA, Hsueh Y-P, Averette AF et al. 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
     [Google Scholar]
  40. 40. 
    Fischer G, James SA, Roberts IN, Oliver SG, Louis EJ 2000. Chromosomal evolution in Saccharomyces. Nature 405:451–54
     [Google Scholar]
  41. 41. 
    Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB et al. 2004. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLOS Biol 2:e384
     [Google Scholar]
  42. 42. 
    Fraser JA, Hsueh Y-P, Findley K, Heitman J 2007. Evolution of the mating-type locus: the basidiomycetes. Sex in Fungi J Heitman, JW Kronstad, JW Taylor, LA Casselton 19–34 Washington, DC: ASM Press
     [Google Scholar]
  43. 43. 
    Fraser JA, Subaran RL, Nichols CB, Heitman J 2003. Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island, Canada. Eukaryot. Cell 2:1036–45
     [Google Scholar]
  44. 44. 
    Fries BC, Chen F, Currie BP, Casadevall A 1996. Karyotype instability in Cryptococcus neoformans infection. J. Clin. Microbiol. 34:1531–34
     [Google Scholar]
  45. 45. 
    Fu C, Heitman J. 2017. PRM1 and KAR5 function in cell-cell fusion and karyogamy to drive distinct bisexual and unisexual cycles in the Cryptococcus pathogenic species complex. PLOS Genet 13:e1007113
     [Google Scholar]
  46. 46. 
    Fu C, Sun S, Billmyre RB, Roach KC, Heitman J 2014. Unisexual versus bisexual mating in Cryptococcus neoformans: consequences and biological impacts. Fungal Genet. Biol. 78:65–75
     [Google Scholar]
  47. 47. 
    Gerstein AC, Fu MS, Mukaremera L, Li Z, Ormerod KL et al. 2015. Polyploid titan cells produce haploid and aneuploid progeny to promote stress adaptation. mBio 6:e01340–15
     [Google Scholar]
  48. 48. 
    Giles SS, Dagenais TRT, Botts MR, Keller NP, Hull CM 2009. Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect. Immun 77:3491–500
     [Google Scholar]
  49. 49. 
    Gioti A, Nystedt B, Li W, Xu J, Andersson A et al. 2013. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. mBio 4:e00572–12
     [Google Scholar]
  50. 50. 
    Goodenough U, Heitman J. 2014. Origins of eukaryotic sexual reproduction. Cold Spring Harb. Perspect. Biol. 6:a016154
     [Google Scholar]
  51. 51. 
    Greig D, Travisano M, Louis EJ, Borts RH 2003. A role for the mismatch repair system during incipient speciation in Saccharomyces. J. Evol. Biol 16:429–37
     [Google Scholar]
  52. 52. 
    Guerreiro MA, Springer DJ, Rodrigues JA, Rusche LN, Findley K et al. 2013. Molecular and genetic evidence for a tetrapolar mating system in the basidiomycetous yeast Kwoniella mangrovensis and two novel sibling species. Eukaryot. Cell 12:746–60
     [Google Scholar]
  53. 53. 
    Gyawali R, Lin X. 2011. Mechanisms of uniparental mitochondrial DNA inheritance in Cryptococcus neoformans. Mycobiology 39:235–42
     [Google Scholar]
  54. 54. 
    Gyawali R, Lin X. 2013. Prezygotic and postzygotic control of uniparental mitochondrial DNA inheritance in Cryptococcus neoformans. mBio 4:e00112–13
     [Google Scholar]
  55. 55. 
    Gyawali R, Zhao Y, Lin J, Fan Y, Xu X et al. 2017. Pheromone independent unisexual development in Cryptococcus neoformans. PLOS Genet 13:e1006772
     [Google Scholar]
  56. 56. 
    Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I et al. 2015. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet. Biol. 78:16–48
     [Google Scholar]
  57. 57. 
    Heitman J. 2015. Evolution of sexual reproduction: A view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol. Rev. 29:108–17
     [Google Scholar]
  58. 58. 
    Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR, eds. 2018. The Fungal Kingdom Washington, DC: ASM Press
  59. 59. 
    Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A, eds. 2011. Cryptococcus: From Human Pathogen to Model Yeast Washington, DC: ASM Press
  60. 60. 
    Heitman J, Kronstad JW, Taylor JW, Casselton LA, eds. 2007. Sex in Fungi Washington, DC: ASM Press
  61. 61. 
    Heitman J, Sun S, James TY 2013. Evolution of fungal sexual reproduction. Mycologia 105:1–27
     [Google Scholar]
  62. 62. 
    Hiremath SS, Chowdhary A, Kowshik T, Randhawa HS, Sun S, Xu J 2008. Long-distance dispersal and recombination in environmental populations of Cryptococcusneoformans var. grubii from India. Microbiology 154:1513–24
     [Google Scholar]
  63. 63. 
    Homer CM, Summers DK, Goranov AI, Clarke SC, Wiesner DL et al. 2016. Intracellular action of a secreted peptide required for fungal virulence. Cell Host Microbe 19:849–64
     [Google Scholar]
  64. 64. 
    Hommel B, Mukaremera L, Cordero RJB, Coelho C, Desjardins CA et al. 2018. Titan cells formation in Cryptococcus neoformans is finely tuned by environmental conditions and modulated by positive and negative genetic regulators. PLOS Pathog 14:e1006982
     [Google Scholar]
  65. 65. 
    Hou J, Friedrich A, de Montigny J, Schacherer J 2014. Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae. Curr. Biol 24:1153–59
     [Google Scholar]
  66. 66. 
    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 7:1847–55
     [Google Scholar]
  67. 67. 
    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
     [Google Scholar]
  68. 68. 
    Hsueh Y-P, Metin B, Findley K, Rodriguez-Carres M, Heitman J 2011. The mating type locus of Cryptococcus: evolution of gene clusters governing sex determination and sexual reproduction from the phylogenomic perspective. Cryptococcus: From Human Pathogen to Model Yeast J Heitman, TR Kozel, KJ Kwon-Chung, JR Perfect, A Casadevall 139–49 Washington, DC: ASM Press
     [Google Scholar]
  69. 69. 
    Hsueh Y-P, Xue C, Heitman J 2009. A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J 28:1220–33
     [Google Scholar]
  70. 70. 
    Huang M, Hebert AS, Coon JJ, Hull CM 2015. Protein composition of infectious spores reveals novel sexual development and germination factors in Cryptococcus. PLOS Genet 11:e1005490
     [Google Scholar]
  71. 71. 
    Hull CM, Boily MJ, Heitman J 2005. Sex-specific homeodomain proteins Sxi1α and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot. Cell 4:526–35
     [Google Scholar]
  72. 72. 
    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 16:3046–60
     [Google Scholar]
  73. 73. 
    Hunter N, Chambers SR, Louis EJ, Borts RH 1996. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J 15:1726–33
     [Google Scholar]
  74. 74. 
    Idnurm A, Heitman J. 2005. Light controls growth and development via a conserved pathway in the fungal kingdom. PLOS Biol 3:e95
     [Google Scholar]
  75. 75. 
    Idnurm A, Heitman J. 2005. Photosensing fungi: phytochrome in the spotlight. Curr. Biol. 15:R829–32
     [Google Scholar]
  76. 76. 
    Jaco I, Canela A, Vera E, Blasco MA 2008. Centromere mitotic recombination in mammalian cells. J. Cell Biol. 181:885–92
     [Google Scholar]
  77. 77. 
    Janbon G, Ormerod KL, Paulet D, Byrnes EJ III, Yadav V et al. 2014. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLOS Genet 10:e1004261
     [Google Scholar]
  78. 78. 
    Jung K-W, Kim S-Y, Okagaki LH, Nielsen K, Bahn Y-S 2011. Ste50 adaptor protein governs sexual differentiation of Cryptococcus neoformans via the pheromone-response MAPK signaling pathway. Fungal Genet. Biol. 48:154–65
     [Google Scholar]
  79. 79. 
    Karos M, Chang YC, McClelland CM, Clarke DL, Fu J et al. 2000. Mapping of the Cryptococcus neoformans MATα locus: presence of mating type-specific mitogen-activated protein kinase cascade homologs. J. Bacteriol. 182:6222–27
     [Google Scholar]
  80. 80. 
    Kent CR, Ortiz-Bermúdez P, Giles SS, Hull CM 2008. Formulation of a defined V8 medium for induction of sexual development of Cryptococcus neoformans. Appl. Environ. Microbiol 74:6248–53
     [Google Scholar]
  81. 81. 
    Klepser ME, Pfaller MA. 1998. Variation in electrophoretic karyotype and antifungal susceptibility of clinical isolates of Cryptococcus neoformans at a university-affiliated teaching hospital from 1987 to 1994. J. Clin. Microbiol. 36:3653–56
     [Google Scholar]
  82. 82. 
    Klutts JS, Levery SB, Doering TL 2007. A β-1,2-xylosyltransferase from Cryptococcus neoformans defines a new family of glycosyltransferases. J. Biol. Chem. 282:17890–99
     [Google Scholar]
  83. 83. 
    Kothe E. 1996. Tetrapolar fungal mating types: sexes by the thousands. FEMS Microbiol. Rev. 18:65–87
     [Google Scholar]
  84. 84. 
    Kronstad JW, Leong SA. 1990. The b mating-type locus of Ustilago maydis contains variable and constant regions. Genes Dev 4:1384–95
     [Google Scholar]
  85. 85. 
    Kruzel EK, Giles SS, Hull CM 2012. Analysis of Cryptococcus neoformans sexual development reveals rewiring of the pheromone response network by a change in transcription factor identity. Genetics 191:435–49
     [Google Scholar]
  86. 86. 
    Kües U, Casselton LA. 1992. Homeodomains and regulation of sexual development in basidiomycetes. Trends Genet 8:154–55
     [Google Scholar]
  87. 87. 
    Kües U, James TY, Heitman J 2011. Mating type in basidiomycetes: unipolar, bipolar, and tetrapolar patterns of sexuality. The Mycota: Evolution of Fungi and Fungal-Like Organisms S Pöggeler, J Wöstemeyer 1497–160 Berlin: Springer
     [Google Scholar]
  88. 88. 
    Kwon-Chung KJ. 1975. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67:1197–200
     [Google Scholar]
  89. 89. 
    Kwon-Chung KJ. 1976. A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 68:943–46
     [Google Scholar]
  90. 90. 
    Kwon-Chung KJ. 1976. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68:821–33
     [Google Scholar]
  91. 91. 
    Kwon-Chung KJ. 2011. Filobasidiella. The Yeasts: A Taxonomic Study CP Kurtzman, JW Fell, T Boekhout 31443–55 Amsterdam: Elsevier Science. , 5th ed..
     [Google Scholar]
  92. 92. 
    Kwon-Chung KJ, Bennett JE. 1978. Distribution of α and α mating types of Cryptococcus neoformans among natural and clinical isolates. Am. J. Epidemiol. 108:337–40
     [Google Scholar]
  93. 93. 
    Kwon-Chung KJ, Bennett JE, Wickes BL, Meyer W, Cuomo CA et al. 2017. The case for adopting the “species complex” nomenclature for the etiologic agents of cryptococcosis. mSphere 2:e00357–16
     [Google Scholar]
  94. 94. 
    Kwon-Chung KJ, Edman JC, Wickes BL 1992. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun 60:602–5
     [Google Scholar]
  95. 95. 
    Lee H, Chang YC, Nardone G, Kwon-Chung KJ 2007. TUP1 disruption in Cryptococcus neoformans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quorum sensing. Mol. Microbiol. 64:591–601
     [Google Scholar]
  96. 96. 
    Lee SC, Heitman J. 2012. Function of Cryptococcus neoformans KAR7 (SEC66) in karyogamy during unisexual and opposite-sex mating. Eukaryot. Cell 11:783–94
     [Google Scholar]
  97. 97. 
    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
     [Google Scholar]
  98. 98. 
    Lengeler KB, Cox GM, Heitman J 2001. Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect. Immun. 69:115–22
     [Google Scholar]
  99. 99. 
    Lengeler KB, Fox DS, Fraser JA, Allen A, Forrester K et al. 2002. Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot. Cell 1:704–18
     [Google Scholar]
  100. 100. 
    Lin J, Idnurm A, Lin X 2015. Morphology and its underlying genetic regulation impact the interaction between Cryptococcus neoformans and its hosts. Med. Mycol. 53:493–504
     [Google Scholar]
  101. 101. 
    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
     [Google Scholar]
  102. 102. 
    Lin X, Hull CM, Heitman J 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:1017–21
     [Google Scholar]
  103. 103. 
    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
     [Google Scholar]
  104. 104. 
    Lin X, Litvintseva AP, Nielsen K, Patel S, Floyd A et al. 2007. αADα hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLOS Genet 3:1975–90
     [Google Scholar]
  105. 105. 
    Lin X, Nielsen K, Patel S, Heitman J 2008. Impact of mating type, serotype, and ploidy on the virulence of Cryptococcus neoformans. Infect. Immun 76:2923–38
     [Google Scholar]
  106. 106. 
    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 Pathog 5:e1000283
     [Google Scholar]
  107. 107. 
    Liti G, Barton DB, Louis EJ 2006. Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174:839–50
     [Google Scholar]
  108. 108. 
    Litvintseva AP, Kestenbaum L, Vilgalys R, Mitchell TG 2005. Comparative analysis of environmental and clinical populations of Cryptococcus neoformans. J. Clin. Microbiol 43:556–64
     [Google Scholar]
  109. 109. 
    Litvintseva AP, Marra RE, Nielsen K, Heitman J, Vilgalys R, Mitchell TG 2003. Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot. Cell 2:1162–68
     [Google Scholar]
  110. 110. 
    Liu XZ, Wang QM, Goker M, Groenewald M, Kachalkin AV et al. 2015. Towards an integrated phylogenetic classification of the Tremellomycetes. Stud. Mycol. 81:85–147
     [Google Scholar]
  111. 111. 
    Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P et al. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321–24
     [Google Scholar]
  112. 112. 
    Lugarini C, Goebel CS, Condas LAZ, Muro MD, de Farias MR et al. 2008. Cryptococcus neoformans isolated from passerine and psittacine bird excreta in the state of Paraná, Brazil. Mycopathologia 166:61–69
     [Google Scholar]
  113. 113. 
    Magditch DA, Liu T-B, Xue C, Idnurm A 2012. DNA mutations mediate microevolution between host-adapted forms of the pathogenic fungus Cryptococcus neoformans. PLOS Pathog 8:e1002936
     [Google Scholar]
  114. 114. 
    Malik R, Krockenberger MB, Cross G, Doneley R, Madill DN et al. 2003. Avian cryptococcosis. Med. Mycol. 41:115–24
     [Google Scholar]
  115. 115. 
    Maloisel L, Rossignol JL. 1998. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev 12:1381–89
     [Google Scholar]
  116. 116. 
    McClelland CM, Fu J, Woodlee GL, Seymour TS, Wickes BL 2002. Isolation and characterization of the Cryptococcus neoformans MATa pheromone gene. Genetics 160:935–47
     [Google Scholar]
  117. 117. 
    Mead ME, Hull CM. 2016. Transcriptional control of sexual development in Cryptococcus neoformans. J. Microbiol 54:339–46
     [Google Scholar]
  118. 118. 
    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:e10000961
     [Google Scholar]
  119. 119. 
    Moore TDE, Edman JC. 1993. The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol. Cell. Biol. 13:1962–70
     [Google Scholar]
  120. 120. 
    Neilson JB, Ivey MH, Bulmer GS 1978. Cryptococcus neoformans: pseudohyphal forms surviving culture with Acanthamoeba polyphaga. Infect. Immun 20:262–66
     [Google Scholar]
  121. 121. 
    Ni M, Feretzaki M, Li W, Floyd-Averette A, Mieczkowski P et al. 2013. Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLOS Biol 11:e1001653
     [Google Scholar]
  122. 122. 
    Ni M, Feretzaki M, Sun S, Wang X, Heitman J 2011. Sex in fungi. Annu. Rev. Genet. 45:405–30
     [Google Scholar]
  123. 123. 
    Nichols CB, Fraser JA, Heitman J 2004. PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating in Cryptococcus neoformans. Mol. Biol. Cell 15:4476–89
     [Google Scholar]
  124. 124. 
    Nielsen K, Cox GM, Litvintseva AP, Mylonakis E, Malliaris SD et al. 2005. Cryptococcus neoformans α strains preferentially disseminate to the central nervous system during coinfection. Infect. Immun. 73:4922–33
     [Google Scholar]
  125. 125. 
    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. 71:4831–41
     [Google Scholar]
  126. 126. 
    Nielsen K, De Obaldia AL, Heitman J 2007. Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot. Cell 6:949–59
     [Google Scholar]
  127. 127. 
    O'Brien CR, Krockenberger MB, Wigney DI, Martin P, Malik R 2004. Retrospective study of feline and canine cryptococcosis in Australia from 1981 to 2001: 195 cases. Med. Mycol. 42:449–60
     [Google Scholar]
  128. 128. 
    Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ et al. 2010. Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLOS Pathog 6:e1000953
     [Google Scholar]
  129. 129. 
    Okagaki LH, Wang Y, Ballou ER, O'Meara TR, Bahn Y-S et al. 2011. Cryptococcal titan cell formation is regulated by G-protein signaling in response to multiple stimuli. Eukaryot. Cell 10:1306–16
     [Google Scholar]
  130. 130. 
    O'Meara TR, Alspaugh JA. 2012. The Cryptococcus neoformans capsule: a sword and a shield. Clin. Microbiol. Rev. 25:387–408
     [Google Scholar]
  131. 131. 
    Paoletti M, Buck KW, Brasier CM 2006. Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol. Ecol 15:249–62
     [Google Scholar]
  132. 132. 
    Passer AR, Coelho MA, Billmyre RB, Nowrousian M, Mittelbach M et al. 2019. Genetic and genomic analyses reveal boundaries between species closely related to Cryptococcus pathogens. mBio 10:e00764–19
     [Google Scholar]
  133. 133. 
    Perfect JR, Ketabchi N, Cox GM, Ingram CW, Beiser CL 1993. Karyotyping of Cryptococcus neoformans as an epidemiological tool. J. Clin. Microbiol. 31:3305–9
     [Google Scholar]
  134. 134. 
    Polacheck I, Lebens GA. 1989. Electrophoretic karyotype of the pathogenic yeast Cryptococcus neoformans. J. Gen. Microbiol 135:65–71
     [Google Scholar]
  135. 135. 
    Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP et al. 2017. Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect. Dis. 17:873–81
     [Google Scholar]
  136. 136. 
    Randhawa HS, Kowshik T, Chowdhary A, Preeti Sinha K, Khan ZU et al. 2008. The expanding host tree species spectrum of Cryptococcus gattii and Cryptococcus neoformans and their isolations from surrounding soil in India. Med. Mycol. 46:823–33
     [Google Scholar]
  137. 137. 
    Raper JR. 1966. Genetics of Sexuality in Higher Fungi New York: Ronald Press Co.
  138. 138. 
    Raudaskoski M, Kothe E. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryot. Cell 9:847–59
     [Google Scholar]
  139. 139. 
    Rayssiguier C, Thaler DS, Radman M 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 23:396–401
     [Google Scholar]
  140. 140. 
    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 5:1065–80
     [Google Scholar]
  141. 141. 
    Rhodes J, Desjardins CA, Sykes SM, Beale MA, Vanhove M et al. 2017. Tracing genetic exchange and biogeography of Cryptococcus neoformans at the global population level. Genetics 207:327–46
     [Google Scholar]
  142. 142. 
    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
     [Google Scholar]
  143. 143. 
    Roeder GS. 1997. Meiotic chromosomes: It takes two totango. Genes Dev 11:2600–21
     [Google Scholar]
  144. 144. 
    Rogers DW, McConnell E, Ono J, Greig D 2018. Spore-autonomous fluorescent protein expression identifies meiotic chromosome mis-segregation as the principal cause of hybrid sterility in yeast. PLOS Biol 16:e2005066
     [Google Scholar]
  145. 145. 
    Roth C, Sun S, Billmyre RB, Heitman J, Magwene PM 2018. A high resolution map of meiotic recombination in Cryptococcus deneoformans demonstrates decreased recombination in unisexual reproduction. Genetics 209:567–78
     [Google Scholar]
  146. 146. 
    Sankaranarayanan SR, Ianiri G, Reza MH, Thimmappa BC, Ganguly P et al. 2019. Centromere-mediated chromosome break drives karyotype evolution in closely related Malassezia species. bioRxiv 533794. https://doi.org/10.1101/533794
    [Crossref]
  147. 147. 
    Sharpton TJ, Neafsey DE, Galagan JE, Taylor JW 2008. Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 9:R24
     [Google Scholar]
  148. 148. 
    Shen WC, Davidson RC, Cox GM, Heitman J 2002. Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans. Eukaryot. Cell 1:366–77
     [Google Scholar]
  149. 149. 
    Shi J, Wolf SE, Burke JM, Presting GG, Ross-Ibarra J, Dawe RK 2010. Widespread gene conversion in centromere cores. PLOS Biol 8:e1000327
     [Google Scholar]
  150. 150. 
    Sia RA, Lengeler KB, Heitman J 2000. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet. Biol. 29:153–63
     [Google Scholar]
  151. 151. 
    Singer LM, Meyer W, Firacative C, Thompson GR, Samitz E, Sykes JE 2014. Antifungal drug susceptibility and phylogenetic diversity among Cryptococcus isolates from dogs and cats in North America. J. Clin. Microbiol. 52:2061–70
     [Google Scholar]
  152. 152. 
    Staib F. 1981. The perfect state of Cryptococcus neoformans, Filobasidiella neoformans, on pigeon manure filtrate agar. Zentralbl. Bakteriol. A 248:575–78
     [Google Scholar]
  153. 153. 
    Steenbergen JN, Shuman HA, Casadevall A 2001. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. PNAS 98:15245–50
     [Google Scholar]
  154. 154. 
    Sun S, Billmyre RB, Mieczkowski P, Heitman J 2014. Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans. PLOS Genet 10:e1004849
     [Google Scholar]
  155. 155. 
    Sun S, Heitman J. 2015. From two to one: unipolar sexual reproduction. Fungal Biol. Rev. 29:118–25
     [Google Scholar]
  156. 156. 
    Sun S, Heitman J. 2016. Running hot and cold: recombination around and within mating-type loci of fungi and other eukaryotes. Environmental and Microbial Relationships SI Druzhinina, PC Kubicek 3–13 Cham, Switz.: Springer Int. Publ.
     [Google Scholar]
  157. 157. 
    Sun S, Hsueh Y-P, Heitman J 2012. Gene conversion occurs within the mating-type locus of Cryptococcus neoformans during sexual reproduction. PLOS Genet 8:e1002810
     [Google Scholar]
  158. 158. 
    Sun S, Xu J. 2007. Genetic analyses of a hybrid cross between serotypes A and D strains of the human pathogenic fungus Cryptococcus neoformans. Genetics 177:1475–86
     [Google Scholar]
  159. 159. 
    Sun S, Xu J. 2009. Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLOS ONE 4:e5524
     [Google Scholar]
  160. 160. 
    Sun S, Yadav V, Billmyre RB, Cuomo CA, Nowrousian M et al. 2017. Fungal genome and mating system transitions facilitated by chromosomal translocations involving intercentromeric recombination. PLOS Biol 15:e2002527
     [Google Scholar]
  161. 161. 
    Symington LS, Petes TD. 1988. Meiotic recombination within the centromere of a yeast chromosome. Cell 52:237–40
     [Google Scholar]
  162. 162. 
    Termolino P, Cremona G, Consiglio MF, Conicella C 2016. Insights into epigenetic landscape of recombination-free regions. Chromosoma 125:301–8
     [Google Scholar]
  163. 163. 
    Tian X, He G-J, Hu P, Chen L, Tao C et al. 2018. Cryptococcus neoformans sexual reproduction is controlled by a quorum sensing peptide. Nat. Microbiol. 3:698–707
     [Google Scholar]
  164. 164. 
    Trevijano-Contador N, de Oliveira HC, García-Rodas R, Rossi SA, Llorente I et al. 2018. Cryptococcus neoformans can form titan-like cells in vitro in response to multiple signals. PLOS Pathog 14:e1007007
     [Google Scholar]
  165. 165. 
    Velagapudi R, Hsueh Y-P, Geunes-Boyer S, Wright JR, Heitman J 2009. Spores as infectious propagules of Cryptococcus neoformans. Infect. Immun 77:4345–55
     [Google Scholar]
  166. 166. 
    Wang L, Tian X, Gyawali R, Upadhyay S, Foyle D et al. 2014. Morphotype transition and sexual reproduction are genetically associated in a ubiquitous environmental pathogen. PLOS Pathog 10:e1004185
     [Google Scholar]
  167. 167. 
    Wang L, Zhai B, Lin X 2012. The link between morphotype transition and virulence in Cryptococcus neoformans. PLOS Pathog 8:e1002765
     [Google Scholar]
  168. 168. 
    Wang P, Heitman J. 1999. Signal transduction cascades regulating mating, filamentation, and virulence in Cryptococcus neoformans. Curr. Opin. Microbiol 2:358–62
     [Google Scholar]
  169. 169. 
    Wang P, Nichols CB, Lengeler KB, Cardenas ME, Cox GM et al. 2002. Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot. Cell 1:257–72
     [Google Scholar]
  170. 170. 
    Wang X, Darwiche S, Heitman J 2013. Sex-induced silencing operates during opposite-sex and unisexual reproduction in Cryptococcus neoformans. Genetics 193:1163–74
     [Google Scholar]
  171. 171. 
    Wang X, Hsueh Y-P, Li W, Floyd A, Skalsky R, Heitman J 2010. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev 24:2566–82
     [Google Scholar]
  172. 172. 
    Wickes BL, Moore TDE, Kwon-Chung KJ 1994. Comparison of the electrophoretic karyotypes and chromosomal location of ten genes in the two varieties of Cryptococcus neoformans. Microbiology 140:543–50
     [Google Scholar]
  173. 173. 
    Williamson PR. 1997. Laccase and melanin in the pathogenesis of Cryptococcus neoformans. Front. Biosci 2:e99–107
     [Google Scholar]
  174. 174. 
    Xu J, Ali RY, Gregory DA, Amick D, Lambert SE et al. 2000. Uniparental mitochondrial transmission in sexual crosses in Cryptococcus neoformans. Curr. Microbiol 40:269–73
     [Google Scholar]
  175. 175. 
    Xu J, Luo G, Vilgalys RJ, Brandt ME, Mitchell TG 2002. Multiple origins of hybrid strains of Cryptococcus neoformans with serotype AD. Microbiology 148:203–12
     [Google Scholar]
  176. 176. 
    Xu J, Vilgalys R, Mitchell TG 2000. Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol. Ecol 9:1471–81
     [Google Scholar]
  177. 177. 
    Xu X, Lin J, Zhao Y, Kirkman E, So Y-S et al. 2017. Glucosamine stimulates pheromone-independent dimorphic transition in Cryptococcus neoformans by promoting Crz1 nuclear translocation. PLOS Genet 13:e1006982
     [Google Scholar]
  178. 178. 
    Xue C. 2012. Cryptococcus and beyond—inositol utilization and its implications for the emergence of fungal virulence. PLOS Pathog 8:e1002869
     [Google Scholar]
  179. 179. 
    Xue C, Tada Y, Dong X, Heitman J 2007. The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1:263–73
     [Google Scholar]
  180. 180. 
    Yadav V, Sun S, Billmyre RB, Thimmappa BC, Shea T et al. 2018. RNAi is a critical determinant of centromere evolution in closely related fungi. PNAS 115:3108–13
     [Google Scholar]
  181. 181. 
    Yan Z, Hull CM, Heitman J, Sun S, Xu J 2004. SXI1α controls uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr. Biol 14:R743–44
     [Google Scholar]
  182. 182. 
    Yan Z, Hull CM, Sun S, Heitman J, Xu JP 2007. The mating type-specific homeodomain genes SXI1α and SXI2a coordinately control uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr. Genet 51:187–95
     [Google Scholar]
  183. 183. 
    Yan Z, Sun S, Shahid M, Xu J 2007. Environment factors can influence mitochondrial inheritance in the fungus Cryptococcus neoformans. Fungal Genet. Biol 44:315–22
     [Google Scholar]
  184. 184. 
    Yan Z, Xu J. 2003. Mitochondria are inherited from the MATa parent in crosses of the basidiomycete fungus Cryptococcus neoformans. Genetics 163:1315–25
     [Google Scholar]
  185. 185. 
    Yue C, Cavallo LM, Alspaugh JA, Wang P, Cox GM et al. 1999. The STE12α homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 153:1601–15
     [Google Scholar]
  186. 186. 
    Zhai B, Wozniak KL, Masso-Silva J, Upadhyay S, Hole C et al. 2015. Development of protective inflammation and cell-mediated immunity against Cryptococcus neoformans after exposure to hyphal mutants. mBio 6:e01433-15
     [Google Scholar]
  187. 187. 
    Zhao Y, Upadhyay S, Lin X 2018. PAS domain protein Pas3 interacts with the chromatin modifier Bre1 in regulating cryptococcal morphogenesis. mBio 9:e02135–18
     [Google Scholar]
  188. 188. 
    Zhu Y, Engström PG, Tellgren-Roth C, Baudo CD, Kennell JC et al. 2017. Proteogenomics produces comprehensive and highly accurate protein-coding gene annotation in a complete genome assembly of Malassezia sympodialis. Nucleic Acids Res 45:2629–43
     [Google Scholar]
  189. 189. 
    Zimmer BL, Hempel HO, Goodman NL 1984. Pathogenicity of the basidiospores of Filobasidiella neoformans. Mycopathologia 85:149–53
     [Google Scholar]
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The Evolution of Sexual Reproduction and the Mating-Type Locus: Links to Pathogenesis of Cryptococcus Human Pathogenic Fungi
Annual Review of Genetics 53, 417 (2019); https://doi.org/10.1146/annurev-genet-120116-024755
/content/journals/10.1146/annurev-genet-120116-024755
/content/journals/10.1146/annurev-genet-120116-024755
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