Mechanisms of unisexual mating in Cryptococcus neoformans

Fungal Genetics and Biology

Volumn 48, Issue 7, 2011, Pages 651-660

  Wang, Linqi ^a   Lin, Xiaorong ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Bisexual mating; Dimorphism; MAT locus; Monokaryotic fruiting; Unisexual mating; Virulence

Indexed keywords

BISEXUALITY; CANDIDA ALBICANS; CPR2 GENE; CRYPTOCOCCUS NEOFORMANS; ENVIRONMENTAL FACTOR; FUNGAL COLONIZATION; FUNGAL GENE; FUNGAL GENETICS; FUNGAL PHENOMENA AND FUNCTIONS; FUNGAL STRAIN; FUNGAL SURVIVAL; FUNGAL VIRULENCE; FUNGUS HYPHAE; FUNGUS ISOLATION; HOST PATHOGEN INTERACTION; MATING SYSTEM; MICROBIAL ACTIVITY; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NONHUMAN; PARTHENOGENESIS; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; STE12 GENE; STE3 GENE; ZNF2 GENE;

ADAPTATION, BIOLOGICAL; CRYPTOCOCCUS NEOFORMANS; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; RECOMBINATION, GENETIC;

ANIMALIA; EUKARYOTA; FILOBASIDIELLA NEOFORMANS;

EID: 79956080192     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.02.001     Document Type: Review

References (147)

1. Alby K., et al. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 2009, 460:890-893.
2. Alspaugh J.A., et al. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 1997, 11:3206-3217.
3. Alspaugh J.A., et al. Morphogenesis of Cryptococcus neoformans. Contrib. Microbiol. 2000, 5:217-238.
4. Bahn Y.S., et al. Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr. Biol. 2005, 15:2013-2020.
5. Bahn Y.S., et al. Ssk2 mitogen-activated protein kinase kinase kinase governs divergent patterns of the stress-activated Hog1 signaling pathway in Cryptococcus neoformans. Eukaryot Cell. 2007, 6:2278-2289.
6. Banerjee M., et al. UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol. Biol. Cell 2008, 19:1354-1365.
7. Belay T., et al. Serotyping of Cryptococcus neoformans by dot enzyme assay. J. Clin. Microbiol. 1996, 34:466-470.
8. Bennett R.J. A Candida-based view of fungal sex and pathogenesis. Genome Biol. 2009, 10:230.
9. Bennett R.J., Johnson A.D. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 2003, 22:2505-2515.
10. Biggs R. Cultural studies in the Thelephoraceae and related fungi. Mycologia 1938, 30:64-78.
11. Bogomolnaya L.M., et al. Roles of the RAM signaling network in cell cycle progression in Saccharomyces cerevisiae. Curr. Genet. 2006, 49:384-392.
12. Botts M.R., et al. Isolation and characterization of Cryptococcus neoformans spores reveal a critical role for capsule biosynthesis genes in spore biogenesis. Eukaryot Cell. 2009, 8:595-605.
13. Bui T., et al. Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, alpha mating type populations. Eukaryot Cell. 2008, 7:1771-1780.
14. Byrnes E.J., et al. Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog. 2010, 6:e1000850.
15. Carlisle P.L., et al. Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc. Natl. Acad. Sci. USA 2009, 106:599-604.
16. Cerikcioglu N. Mating types, sexual reproduction and ploidy in fungi: effects on virulence. Mikrobiyol. Bull. 2009, 43:507-513.
17. Chang Y.C., et al. Cryptococcus neoformans STE12alpha regulates virulence but is not essential for mating. J. Exp. Med. 2000, 191:871-882.
18. Chung S., et al. Molecular analysis of CPRalpha, a MATalpha-specific pheromone receptor gene of Cryptococcus neoformans. Eukaryot Cell. 2002, 1:432-439.
19. Cogliati M., et al. Cryptococcus neoformans population includes hybrid strains homozygous at mating-type locus. FEMS Yeast Res. 2006, 6:608-613.
20. Cruickshank J.G., et al. Cryptococcus neoformans of unusual morphology. Appl. Microbiol. 1973, 25:309-312.
21. Cruz M.C., et al. Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J. 2001, 20:1020-1032.
22. Currie B., et al. Cryptococcus neoformans var gattii. Lancet 1990, 336:1442.
23. Davidson R.C., et al. 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. 2003, 49:469-485.
24. Dumitru R., et al. In vivo and in vitro anaerobic mating in Candida albicans. Eukaryot Cell. 2007, 6:465-472.
25. Dyer P.S., et al. Genomics reveals sexual secrets of Aspergillus. Microbiology 2003, 149:2301-2303.
26. Ekena J.L., et al. Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factors Sxi1alpha and Sxi2a. Eukaryot Cell. 2008, 7:49-57.
27. Elliott T.J. Developmental genetics - from spore to sporephore. Developmental Biology of Higher Fungi 1985, 451-465. Cambridge University Press, Cambridge, UK. D. Moore (Ed.).
28. Erke K.H. Light microscopy of basidia, basidiospores, and nuclei in spores and hyphae of Filobasidiella neoformans (Cryptococcus neoformans). J. Bacteriol. 1976, 128:445-455.
29. Erke K.H., Schneidau J.D. Relationship of some Cryptococcus neoformans hypha-forming strains to standard strains and to other species of yeasts as determined by deoxyribonucleic acid base ratios and homologies. Infect. Immun. 1973, 7:941-948.
30. Forche A., et al. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 2008, 6:e110.
31. Fox D.S., et al. Phospholipid-binding protein Cts1 controls septation and functions coordinately with calcineurin in Cryptococcus neoformans. Eukaryot Cell. 2003, 2:1025-1035.
32. Fraser J.A., et al. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2004, 2:e384.
33. Fraser J.A., et al. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 2005, 437:1360-1364.
34. Freed E.R., et al. Meningoencephalitis due to hyphae-forming Cryptococcus neoformans. Am. J. Clin. Pathol. 1971, 55:30-33.
35. Galagan J.E., et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438:1105-1115.
36. Galitski T., et al. Ploidy regulation of gene expression. Science 1999, 285:251-254.
37. Gauthier G.M., et al. SREB, a GATA transcription factor that directs disparate fates in Blastomyces dermatitidis including morphogenesis and siderophore biosynthesis. PLoS Pathog. 2010, 6:e1000846.
38. Gazzoni A.F., et al. Atypical micromorphology and uncommon location of cryptococcosis: a histopathologic study using special histochemical techniques (one case report). Mycopathologia 2009, 167:197-202.
39. Glass N.L., Smith M.L. Structure and function of a mating-type gene from the homothallic species Neurospora africana. Mol. Gen. Genet. 1994, 244:401-409.
40. Goddard M.R. Why Bother with Sex? 2007, ASM Press, Washington, DC, pp. 489-506.
41. Goddard M.R., et al. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 2005, 434:636-640.
42. Grimberg B., Zeyl C. The effects of sex and mutation rate on adaptation in test tubes and to mouse hosts by Saccharomyces cerevisiae. Evolution 2005, 59:431-438.
43. Gueho E., et al. Phylogenetic relationships of Cryptococcus neoformans and some related basidiomycetous yeasts determined from partial large subunit rRNA sequences. Anton. Van Leeuw. 1993, 63:175-189.
44. Han K.H., et al. A putative G protein-coupled receptor negatively controls sexual development in Aspergillus nidulans. Mol. Microbiol. 2004, 51:1333-1345.
45. Hanna W.F. Sexual stability in monosporous mycelia of Coprinus lagopus. Ann. Bot. 1928, 42:379-388.
46. Hata K., et al. Cells of different ploidy are often present together in Cryptococcus neoformans strains. Nippon Ishinkin Gakkai Zasshi. 2000, 41:161-167.
47. Heitman J. Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 2006, 16:R711-R725.
48. Heitman J. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe. 2010, 8:86-99.
49. Heitman J. Sex in fungi: molecular determination and evolutionary implications 2007, ASM Press, Washington, D.C.
50. Hernandez R., et al. Two-dimensional reference map of Candida albicans hyphal forms. Proteomics 2004, 4:374-382.
51. Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 1988, 52:536-553.
52. Hicks J., et al. Transposable mating type genes in Saccharomyces cerevisiae. Nature 1979, 282:478-483.
53. Hiremath S.S., et al. Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology 2008, 154:1513-1524.
54. Holbrook E.D., Rappleye C.A. Histoplasma capsulatum pathogenesis: making a lifestyle switch. Curr. Opin. Microbiol. 2008, 11:318-324.
55. Hsueh Y.P., Shen W.C. 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. 2005, 4:147-155.
56. Hsueh Y.P., et al. G protein signaling governing cell fate decisions involves opposing Galpha subunits in Cryptococcus neoformans. Mol. Biol. Cell 2007, 18:3237-3249.
57. Hsueh Y.P., et al. A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J. 2009, 28:1220-1233.
58. Hull C.M., Heitman J. Genetics of Cryptococcus neoformans. Annu. Rev. Genet. 2002, 36:557-615.
59. Hull C.M., Johnson A.D. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 1999, 285:1271-1275.
60. Hull C.M., et al. Evidence for mating of the " asexual" yeast Candida albicans in a mammalian host. Science 2000, 289:307-310.
61. Hull C.M., et al. Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1alpha. Genes Dev. 2002, 16:3046-3060.
62. Hull C.M., et al. Sex-specific homeodomain proteins Sxi1alpha and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot Cell. 2005, 4:526-535.
63. Idnurm A., Heitman J. Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol. 2005, 3:e95.
64. Iwasa M., et al. The two nuclei in the dikaryon of the homobasidiomycete Coprinus cinereus change position after each conjugate division. Fungal Genet. Biol. 1998, 23:110-116.
65. Jung K.W., et al. Ste50 adaptor protein governs sexual differentiation of Cryptococcus neoformans via the pheromone-response MAPK signaling pathway. Fungal Genet. Biol. 2010, 48:154-165.
66. Kavanaugh L.A., et al. Recent evolution of the human pathogen Cryptococcus neoformans by intervarietal transfer of a 14-gene fragment. Mol. Biol. Evol. 2006, 23:1879-1890.
67. Kent C.R., et al. Formulation of a defined V8 medium for induction of sexual development of Cryptococcus neoformans. Appl. Environ. Microbiol. 2008, 74:6248-6253.
68. Klein B.S., Tebbets B. Dimorphism and virulence in fungi. Curr. Opin. Microbiol. 2007, 10:314-319.
69. Kondrashov A.S. The asexual ploidy cycle and the origin of sex. Nature 1994, 370:213-216.
70. Kwon-Chung K.J. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 1975, 67:1197-1200.
71. Kwon-Chung K.J. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 1976, 68:821-833.
72. Kwon-Chung K.J. A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 1976, 68:943-946.
73. Kwon-Chung K.J., Bennett J.E. Distribution of alpha and alpha mating types of Cryptococcus neoformans among natural and clinical isolates. Am. J. Epidemiol. 1978, 108:337-340.
74. Kwon-Chung K.J., et al. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 1992, 60:602-605.
75. Kwon-Chung K.J., et al. The characteristics that differentiate Filobasidiella depauperata from Filobasidiella neoformans. Stud. Mycol. 1995, 38:67-79.
76. Lemke P.A. A reevaluation of homothallism, heterothallism and the species concept in Sistotrema brinkmanni. Mycologia 1969, 60:57-76.
77. Lengeler K.B., et al. Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell. 2002, 1:704-718.
78. Lin X. Cryptococcus neoformans: morphogenesis, infection, and evolution. Infect. Genet. Evol. 2009, 9:401-416.
79. Lin X., Heitman J. The biology of the Cryptococcus neoformans species complex. Annu. Rev. Microbiol. 2006, 60:69-105.
80. Lin X., et al. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 2005, 434:1017-1021.
81. Lin X., et al. Virulence attributes and hyphal growth of C. neoformans are quantitative traits and the MATalpha allele enhances filamentation. PLoS Genet. 2006, 2:e187.
82. Lin X., et al. Alpha AD alpha hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet. 2007, 3:1975-1990.
83. Lin X., et al. Impact of mating type, serotype, and ploidy on the virulence of Cryptococcus neoformans. Infect. Immun. 2008, 76:2923-2938.
84. Lin X., et al. Diploids in the Cryptococcus neoformans serotype A population homozygous for the alpha mating type originate via unisexual mating. PLoS Pathog. 2009, 5:e1000283.
85. Lin X., et al. Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and same-sex mating in Cryptococcus neoformans. PLoS Genet. 2010, 6:e1000953.
86. Litvintseva A.P., et al. Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell. 2003, 2:1162-1168.
87. Liu, K.H., Shen, W.C., 2010. Mating differentiation in Cryptococcus neoformans is negatively regulated by the Crk1 protein kinase. Fungal Genet. Biol.
88. Love G.L., et al. Large Cryptococcus neoformans isolated from brain abscess. J. Clin. Microbiol. 1985, 22:1068-1070.
89. Lott T.J., et al. Towards understanding the evolution of the human commensal yeast Candida albicans. Microbiology 1999, 145(Pt 5):1137-1143.
90. Lurie H.I., Shadomy H.J. Morphological variations of a hypha-forming strain of Cryptococcus neoformans (Coward strain) in tissues of mice. Sabouraudia 1971, 9:10-14.
91. Madhani H.D., Fink G.R. The control of filamentous differentiation and virulence in fungi. Trends Cell Biol. 1998, 8:348-353.
92. Magee B.B., Magee P.T. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 2000, 289:310-313.
93. McClelland C.M., et al. Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol. 2004, 12:208-212.
94. Mitchell T.G., Perfect J.R. Cryptococcosis in the era of AIDS - 100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 1995, 8:515-548.
95. Miyake H., et al. Basidiospore formation in monokaryotic fruiting bodies of a mutant strain of Coprinus macrorhizus. Arch. Microbiol. 1980, 126:207-212.
96. Moore D. Fungal Morphogenesis 1998, Cambridge University Press, Cambridge, New York.
97. Moyes D.L., et al. A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe. 2010, 8:225-235.
98. Murata Y., et al. Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 1998, 149:1753-1761.
99. Nadal M., et al. Dimorphism in fungal plant pathogens. FEMS Microbiol. Lett. 2008, 284:127-134.
100. Nasmyth K.A., Tatchell K. The structure of transposable yeast mating type loci. Cell 1980, 19:753-764.
101. Neill J.M., et al. A comparison of the immunogenicity of weakly encapsulated and of strongly encapsulated strains of Cryptococcus neoformans (Torula histolytica). J. Bacteriol. 1950, 59:263-275.
102. Neilson J.B., et al. Cryptococcus neoformans: pseudohyphal forms surviving culture with Acanthamoeba polyphaga. Infect. Immun. 1978, 20:262-266.
103. Neilson J.B., et al. Pseudohyphal forms of Cryptococcus neoformans: decreased survival in vivo. Mycopathologia 1981, 73:57-59.
104. Nemecek J.C., et al. Global control of dimorphism and virulence in fungi. Science 2006, 312:583-588.
105. Nichols C.B., et al. PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating in Cryptococcus neoformans. Mol. Biol. Cell 2004, 15:4476-4489.
106. Nielsen K., Heitman J. Sex and virulence of human pathogenic fungi. Adv. Genet. 2007, 57:143-173.
107. Oishi K., et al. Timing of DNA replication during the meiotic process in monokaryotic basidiocarps of Coprinus macrorhizus. Arch. Microbiol. 1982, 132:372-374.
108. Okagaki L.H., et al. Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog. 2010, 6:e1000953.
109. Paoletti M., et al. Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr. Biol. 2007, 17:1384-1389.
110. Poggeler S., et al. Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 1997, 147:567-580.
111. Pukkila-Worley R., Mylonakis E. Epidemiology and management of cryptococcal meningitis: developments and challenges. Expert Opin. Pharmacother. 2008, 9:551-560.
112. Raper J.R., Krongelb G.S. Genetic and environmental aspects of fruiting in Schizophyllum commune. Mycologia 1958, 50:707-740.
113. Roberston S.J., et al. Homothallism and heterothallism in Sordaria brevicollis. Mycol. Res. 1998, 102:1215-1223.
114. Rodriguez-Carres M., et al. Morphological and genomic characterization of Filobasidiella depauperata: a homothallic sibling species of the pathogenic cryptococcus species complex. PLoS One 2010, 5:e9620.
115. Rutherford J.C., et al. Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcus neoformans. Eukaryot Cell. 2008, 7:237-246.
116. Rydholm C., et al. Low genetic variation and no detectable population structure in Aspergillus fumigatus compared to closely related Neosartorya species. Eukaryot Cell. 2006, 5:650-657.
117. Saul N., et al. Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell. 2008, 7:727-734.
118. Schwartz D., Staib F. Effect of purines on the formation of the perfect state of Cryptococcus neoformans, Filobasidiella neoformans. Zentralbl. Bakteriol. A 1980, 248:274-280.
119. Shadomy S. Further in vitro studies with 5-fluorocytosine. Infect. Immun. 1970, 2:484-488.
120. Shadomy H.J., Utz J.P. Preliminary studies on a hyphaforming mutant of Cryptococcus neoformans. Mycologia 1966, 58:383-390.
121. Shen W.C., et al. Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans. Eukaryot Cell. 2002, 1:366-377.
122. Sia R.A., et al. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet. Biol. 2000, 29:153-163.
123. Song Y., et al. Role of the RAM network in cell polarity and hyphal morphogenesis in Candida albicans. Mol. Biol. Cell 2008, 19:5456-5477.
124. Stahl U., Esser K. Genetics of fruit body production in higher basidiomycetes. I. Monokaryotic fruiting and its correlation with dikaryotic fruiting in Polyporus ciliatus. Mol. Gen. Genet. 1976, 148:183-197.
125. Staib F., et al. Ocular cryptococcosis - experimental and clinical observations. Zentralbl. Bakteriol. Orig A 1977, 237:378-394.
126. Staudt M.W., et al. Characterizing the role of the microtubule binding protein Bim1 in Cryptococcus neoformans. Fungal Genet. Biol. 2010, 47:310-317.
127. Tscharke R.L., et al. Haploid fruiting in Cryptococcus neoformans is not mating type alpha-specific. Fungal Genet. Biol. 2003, 39:230-237.
128. Turgeon B.G. Application of mating type gene technology to problems in fungal biology. Annu. Rev. Phytopathol. 1998, 36:115-137.
129. Uno I., Ishikawa T. Chemical and genetical control of induction of monokaryotic fruiting bodies in Coprinus macrorhizus. Mol. Gen. Genet. 1971, 113:228-239.
130. Uno I., Ishikawa T. Purification and identification of the fruiting-inducing substances in Coprinus macrorhizus. J. Bacteriol. 1973, 113:1240-1248.
131. Velagapudi R., et al. Spores as infectious propagules of Cryptococcus neoformans. Infect. Immun. 2009, 77:4345-4355.
132. Verrinder-Gibbins A.M., Lu B.C. Induction of normal fruiting on originally monokaryotic cultures of Coprinus cinereus. Trans. Brit. Mycol. Soc. 1984, 82:331-335.
133. Walton F.J., et al. Conserved elements of the RAM signaling pathway establish cell polarity in the basidiomycete Cryptococcus neoformans in a divergent fashion from other fungi. Mol. Biol. Cell 2006, 17:3768-3780.
134. Wang P., et al. The G-protein beta subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell. Biol. 2000, 20:352-362.
135. Wang P., et al. Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot Cell. 2002, 1:257-272.
136. Wang P., et al. Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryot Cell. 2004, 3:1028-1035.
137. Wickes B.L. The role of mating type and morphology in Cryptococcus neoformans pathogenesis. Int. J. Med. Microbiol. 2002, 292:313-329.
138. Wickes B.L., et al. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type. Proc. Natl. Acad. Sci. USA 1996, 93:7327-7331.
139. Wickes B.L., et al. The Cryptococcus neoformans STE12alpha gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol. Microbiol. 1997, 26:951-960.
140. Williamson J.D., et al. Atypical cytomorphologic appearance of Cryptococcus neoformans: a report of five cases. Acta Cytol. 1996, 40:363-370.
141. Xu J. Cost of interacting with sexual partners in a facultative sexual microbe. Genetics 2005, 171:1597-1604.
142. Xue C., et al. The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe. 2007, 1:263-273.
143. Yue C., et al. The STE12alpha homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 1999, 153:1601-1615.
144. Yun S.H., et al. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc. Natl. Acad. Sci. USA 1999, 96:5592-5597.
145. Yun S.H., et al. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet. Biol. 2000, 31:7-20.
146. Zaragoza O., et al. Fungal cell gigantism during mammalian infection. PLoS Pathog. 2010, 6:e1000945.
147. Zeyl C., et al. An evolutionary advantage of haploidy in large yeast populations. Science 2003, 299:555-558.