1887

Chapter 7 : Sexual Reproduction of

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Sexual Reproduction of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816858/9781555815011_Chap07-1.gif /docserver/preview/fulltext/10.1128/9781555816858/9781555815011_Chap07-2.gif

Abstract:

This chapter reviews the discovery of both opposite-sex and unisexual reproduction and illustrates how these pathways are molecularly controlled and the central cell biology questions that remain to be addressed. Fungal sexual reproduction is genetically regulated by the mating-type locus (MAT), a specialized region of the genome that is idiomorphic or allelic between different sexes. Similar to the model fission yeast , mating and meiosis of occur sequentially in response to limitation or specific nutrient cues. Other environmental cues such as light and temperature also affect mating of . Those factors that have been connected to the sexual reproduction of are summarized in the chapter. Furthermore, several species can be isolated from trees and fermenting fruits, suggesting that there might be potential plant-fungus interactions that contribute to sexual reproduction of and in nature. Apart from nutritional cues, other environmental signals also influence sexual reproduction. However, the predominance of the α mating type (>99%) in the population represents a paradox as to how sexual reproduction might occur in this essentially unisexual population. The discovery of same-sex mating in resulted in a paradigm shift in considering how genetic diversity is generated in a unisexual population and the evolutionary role of a unisexual reproductive mode. Moreover, the transitions that occur in the fungal kingdom between heterothallic outbreeding and homothallic inbreeding modes promise to reveal general features by which sexual reproduction enhances fitness and enables evolutionary success throughout biology.

Citation: Hsueh Y, Lin X, Kwon-Chung K, Heitman J. 2011. Sexual Reproduction of , p 81-96. In Heitman J, Kozel T, Kwon-Chung K, Perfect J, Casadevall A (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555816858.ch7

Key Concept Ranking

Scanning Electron Microscopy
0.42421108
Transmission Electron Microscopy
0.4118547
Cryptococcus gattii
0.40697676
0.42421108
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Sexual cycle of . (A) -α opposite-sex mating. and α haploid yeast cells secrete peptide pheromones that trigger -α cell-cell fusion under nutrient-limiting conditions. After fusion, cells switch to filamentous growth, and the two nuclei congress but do not fuse in the resulting dikaryotic hyphae. Clamp cells are formed to ensure that two nuclei are faithfully segregated during hyphal growth. Blastospores (yeast-like cells) can bud from the hyphae and divide mitotically. Some hyphal cells can enlarge and form chlamydospores ( ). In the basidium, two nuclei ( and α) fuse and undergo meiosis to produce four chains of basidiospores. In cases where cell fusion is immediately followed by nuclear fusion between and α haploid yeast cells, heterozygous diploid /α yeast cells are created. These diploid cells produce monokaryotic hyphae with unfused clamp cells. Eventually meiosis occurs in the basidium, and basidiospores with and α mating types are generated. (B) α-α same-sex mating (fruiting). During same-sex mating, cells of one mating type become diploid either by endoduplication or by cell-cell and nuclear fusion. The diploid monokaryotic hyphae form rudimentary clamp connections that do not fuse to the preceding cell. Blastospores and chlamydospores are also produced during fruiting. In the basidium, meiosis occurs and haploid basidiospores are produced in four chains. In an alternative model, haploid α cells produce monokaryotic hyphae with haploid nuclei, and diploidization occurs in the basidium, followed by meiosis to produce spores with only the α mating type.

Citation: Hsueh Y, Lin X, Kwon-Chung K, Heitman J. 2011. Sexual Reproduction of , p 81-96. In Heitman J, Kozel T, Kwon-Chung K, Perfect J, Casadevall A (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555816858.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Factors that affect mating in . Plant materials, copper ions, pigeon guano, nitrogen starvation, V8 juice, IAA, and -inositol are compounds and conditions that promote sexual development of . Light, high temperature (37°C), high CO, and water, on the other hand, are known to inhibit mating.

Citation: Hsueh Y, Lin X, Kwon-Chung K, Heitman J. 2011. Sexual Reproduction of , p 81-96. In Heitman J, Kozel T, Kwon-Chung K, Perfect J, Casadevall A (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555816858.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Signaling cascades that contribute to sexual development of . The pheromone response pathway, cAMP-PKA pathway, Ca-calcineurin pathway, and the ammonium sensor Amt2 all positively regulate sexual development, while the light- and stress-sensing pathways negatively regulate this process (see text for details).

Citation: Hsueh Y, Lin X, Kwon-Chung K, Heitman J. 2011. Sexual Reproduction of , p 81-96. In Heitman J, Kozel T, Kwon-Chung K, Perfect J, Casadevall A (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555816858.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816858.ch07
1. Aimi, T.,, R. Yoshida,, M. Ishikawa,, D. Bao,, and Y. Kitamoto. 2005. Identification and linkage mapping of the genes for the putative homeodomain protein (hox1) and the putative pheromone receptor protein homologue (rcb1) in a bipolar basidiomycete, Pholiota nameko. Curr. Genet. 48:184194.
2. Alspaugh, J. A.,, L. M. Cavallo,, J. R. Perfect,, and J. Heitman. 2000. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol. Microbiol. 36:352365.
3. Alspaugh, J. A.,, J.R. Perfect, and, J. Heitman. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 11:32063217.
4. Alspaugh, J. A.,, R. Pukkila-Worley, T. Harashima,, L.M. Cavallo,, D. Funnell,, G. M Cox,, J. R. Perfect,, J. W. Kronstad,, and J. Heitman. 2002. Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot. Cell 1:7584.
5. Anderson, C. M.,, D.A. Willits,, P.J. Kosted,, E. J Ford,, A. D. Martinez-Espinoza,, and J. E. Sherwood. 1999. Molecular analysis of the pheromone and pheromone receptor genes of Ustilago hordei. Gene 240:8997.
6. Bahn, Y. S.,, G.M. Cox,, J.R. Perfect,, and J. Heitman. 2005. Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr. Biol. 15:20132020.
7. Bahn, Y. S.,, J.K. Hicks,, S. S. Giles, G. M. Cox,, and J. Heitman. 2004. Adenylyl cyclase-associated protein Aca1 regulates virulence and differentiation of Cryptococcus neoformans via the cyclic AMP-protein kinase A cascade. Eukaryot. Cell 3:14761491.
8. Bahn, Y. S.,, K. Kojima,, G.M. Cox,, and J. Heitman. 2005. Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol. Biol. Cell 16:22852300.
9. Bahn, Y. S.,, K. Kojima, G. M. Cox,, and J. Heitman. 2006. A unique fungal two-component system regulates stress responses, drug sensitivity, sexual development, and virulence of Cryptococcus neoformans. Mol. Biol. Cell 17:31223135.
10. Bahn, Y. S.,, C. Xue, A. Idnurm,, J. C. Rutherford,, J. Heitman,, and M. E. Cardenas. 2007. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 5:5769.
11. Banuett, F. 1995. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 29:179208.
12. Bauer, R.,, and F. Oberwinkler. 2004. Cellular basidiomycete-fungus interactions, p. 267279. In A. Varma,, L. Abbott,, D. Werner,, and R. Hampp (ed.), Plant Surface Microbiology. Springer-Verlag, Heidelberg, Germany.
13. Bolker, M., M. Urban, and, R. Kahmann. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441450.
14. Botts, M. R.,, S.S. Giles,, M. A. Gates, T. R. Kozel,, and C. M. Hull. 2009. Isolation and characterization of Cryptococcus neoformans spores reveal a critical role for capsule biosynthesis genes in spore biogenesis. Eukaryot. Cell 8:595605.
15. Bovers, M.,, F. Hagen,, E.E. Kuramae,, M.R. Diaz,, L. Spanjaard,, F. Dromer,, H. L. Hoogveld,, and T. Boekhout. 2006. Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res. 6:599607.
16. Bovers, M.,, F. Hagen,, E.E. Kuramae,, H.L. Hoogveld,, F. Dromer,, G. St-Germain,, and T. Boekhout. 2008. AIDS patient death caused by novel Cryptococcus neoformans × C. gattii hybrid. Emerg. Infect. Dis. 14:11051108.
17. Bui, T.,, X. Lin,, R. Malik,, J. Heitman,, and D. Carter. 2008. Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, α mating type populations. Eukaryot. Cell 7:17711780.
18. Bulmer, G. S. 1990. Twenty-five years with Cryptococcus neoformans. Mycopathologia 109:111122.
19. Burkholder, A. C., and, L. H. Hartwell. 1985. The yeast alpha-factor receptor: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res. 13:84638475.
20. Butler,, G. 2007. The evolution of MAT: the ascomycetes, p. 318. In J. Heitman,, J. W. Kronstad, J. W. Taylor, and L. A. Casselton (ed.), Sex in Fungi. ASM Press, Washington, DC.
21. Campbell, L. T.,, B.J. Currie,, M. Krockenberger,, R. Malik,, W. Meyer,, J. Heitman,, and D. Carter. 2005. Clonality and recombination in genetically differentiated subgroups of Cryptococcus gattii. Eukaryot. Cell 4:14031409.
22. Campbell, L. T.,, J.A. Fraser,, C.B. Nichols,, F. S Dietrich,, D. Carter,, and J. Heitman. 2005. Clinical and environmental isolates of Cryptococcus gattii from Australia that retain sexual fecundity. Eukaryot. Cell 4:14101419.
23. Chang, Y. C., G. F. Miller, and, K. J. Kwon-Chung. 2003. Importance of a developmentally regulated pheromone receptor of Cryptococcus neoformans for virulence. Infect. Immun. 71:49534960.
24. Chang, Y. C., L. A. Penoyer, and, K. J. Kwon-Chung. 2001. The second STE12 homologue of Cryptococcus neoformans is MATa-specific and plays an important role in virulence. Proc. Natl. Acad. Sci. USA 98:32583263.
25. Chang, Y. C.,, B.L. Wickes,, G. F. Miller, L. A. Penoyer,, and K. J. Kwon-Chung. 2000. Cryptococcus neoformans STE12α regulates virulence but is not essential for mating. J. Exp. Med. 191:871882.
26. Chung, S.,, M. Karos,, Y.C. Chang,, J. Lukszo, B. L. Wickes,, and K. J. Kwon-Chung. 2002. Molecular analysis of CPRalpha, a MATalpha-specific pheromone receptor gene of Cryptococcus neoformans. Eukaryot. Cell 1:432439.
27. Clements, R. S., Jr., and, B. Darnell. 1980. Myoinositol content of common foods: development of a high-myoinositol diet. Am. J. Clin. Nutr. 33:19541967.
28. Couve, A., and, J. P. Hirsch. 1996. Loss of sustained Fus3p kinase activity and the G1 arrest response in cells expressing an inappropriate pheromone receptor. Mol. Cell. Biol. 16:44784485.
29. Cruz, M. C.,, D.S. Fox, and, J. Heitman. 2001. Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J. 20:10201032.
30. Davidson, R. C.,, C.B. Nichols,, G. M. Cox, J. R. Perfect,, and J. Heitman. 2003. A MAP kinase cascade composed of cell type specific and non-specific elements controls mating and differentiation of the fungal pathogen Cryptococcus neoformans. Mol. Microbiol. 49:469485.
31. Day, P. R. 1963. Mutations of the A mating type factor in Coprinus lagopus. Genet. Res. Camb. 4:5564.
32. Dohlman, H. G.,, J. Song, D. Ma,, W.E. Courchesne,, and J. Thorner. 1996. Sst2, a negative regulator of pheromone signaling in the yeast Saccharomyces cerevisiae: expression, localization, and genetic interaction and physical association with Gpa1 (the G-protein alpha subunit). Mol. Cell. Biol. 16:51945209.
33. D’Souza, C. A.,, J.A. Alspaugh,, C. Yue,, T. Harashima,, G. M Cox,, J. R. Perfect,, and J. Heitman. 2001. Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol. Cell. Biol. 21:31793191.
34. Ekena, J. L.,, B.C. Stanton,, J. A. Schiebe-Owens,, and C. M. Hull. 2008. Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factors Sxi1alpha and Sxi2a. Eukaryot. Cell 7:4957.
35. Elliott, T. J. 1985. Developmental genetics: from spore to sporephore, p. 451465. In D. Moore,, L. A. Casselton, D. A. Wood, and J. C. Frankland (ed.), Developmental Biology of Higher Fungi. Cambridge University Press, Cambridge, UK.
36. Ellis, D. H., and, T. J. Pfeiffer. 1990. Natural habitat of Cryptococcus neoformans var. gattii. J. Clin. Microbiol. 28:16421644.
37. Erke, K. H. 1976. Light microscopy of basidia, basidiospores, and nuclei in spores and hyphae of Filobasidiella neoformans (Cryptococcus neoformans). J. Bacteriol. 128:445455.
38. Erke, K. H., and, J. D. Schneidau, Jr. 1973. 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. 7:941948.
39. Fell, J. W.,, A.C. Statzell,, I.L. Hunter,, and H. J. Phaff. 1969. Leucosporidium gen. n., the heterobasidiomycetous stage of several yeasts of the genus Candida. Antonie Van Leeuwenhoek 35:433462.
40. Fraser, J. A.,, S. Diezmann, R. L. Subaran,, A. Allen,, K. B Lengeler,, F. S. Dietrich,, and J. Heitman. 2004. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2:e384.
41. Fraser, J. A.,, S.S. Giles,, E. C. Wenink,, S. G. Geunes-Boyer,, J. R Wright,, S. Diezmann,, A. Allen,, J. E Stajich,, F.S. Dietrich,, J. R. Perfect,, and J. Heitman. 2005. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:13601364.
42. Fraser, J. A.,, Y.P. Hsueh,, K.M. Findley,, and J. Heitman. 2007. Evolution of the mating-type locus: the basidiomycetes, p. 1934. In J. Heitman,, J. W. Kronstad,, J. W. Taylor,, and L. A. Casselton (ed.), Sex in Fungi. ASM Press, Washington, DC.
43. Fraser, J. A.,, R.L. Subaran,, C.B. Nichols,, and J. Heitman. 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 2:10361045.
44. Gueho, E.,, L. Improvisi,, R. Christen, and, G. S. de Hoog. 1993. Phylogenetic relationships of Cryptococcus neoformans and some related basidiomycetous yeasts determined from partial large subunit rRNA sequences. Antonie Van Leeuwenhoek 63:175189.
45. Hagen, D. C., G. McCaffrey, and, G. F. Sprague, Jr. 1986. Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc. Natl. Acad. Sci. USA 83:14181422.
46. Hanna, W. F. 1928. Sexual stability in monosporous mycelia of Coprinus lagopus. Ann. Bot. 42:379388.
47. Hatch, T. F. 1961. Distribution and deposition of inhaled particles in respiratory tract. Bacteriol. Rev. 25:237240.
48. Heitman, J. 2006. Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 16:R711725.
49. Herskowitz, I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749757.
50. Herskowitz, I.,, and Y. Oshima. 1981. Control of cell type in Saccharomyces cerevisiae: mating type and mating-type interconversion, p. 181209. In J. N. Strathern,, E. W. Jones,, and J. R. Broach (ed.), The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Hiremath, S. S.,, A. Chowdhary, T. Kowshik,, H. S. Randhawa, S. Sun,, and J. Xu. 2008. Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology 154:15131524.
52. Hirsch, J. P., and, F. R. Cross. 1993. The pheromone receptors inhibit the pheromone response pathway in Saccharomyces cerevisiae by a process that is independent of their associated G alpha protein. Genetics 135:943953.
53. Hoff, B., S. Poggeler, and, U. Kuck. 2008. Eighty years after its discovery, Fleming’s Penicillium strain discloses the secret of its sex. Eukaryot. Cell 7:465470.
54. Hsueh, Y. P., and, J. Heitman. 2008. Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr. Opin. Microbiol. 11:517524.
55. Hsueh, Y. P.,, C. Xue, and, J. Heitman. 2007. G protein signaling governing cell fate decisions involves opposing Galpha subunits in Cryptococcus neoformans. Mol. Biol. Cell 18:32373249.
56. Hsueh, Y. P.,, C. Xue, and, J. Heitman. 2009. A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J. 28:12201233.
57. Hull, C. M.,, M.J. Boily, and, J. Heitman. 2005. Sex-specific homeodomain proteins Sxi1alpha and Sxi2 a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot. Cell 4:526535.
58. Hull, C. M.,, R.C. Davidson, and, J. Heitman. 2002. Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1alpha. Genes Dev. 16:30463060.
59. Hull, C. M., and, J. Heitman. 2002. Genetics of Cryptococcus neoformans. Annu. Rev. Genet. 36:557615.
60. Idnurm, A. 2010. A tetrad analysis of the basidiomycete fungus Cryptococcus neoformans. Genetics 185:153163.
61. Idnurm, A.,, Y.S. Bahn,, K. Nielsen, X. Lin,, J.A. Fraser,, and J. Heitman. 2005. Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat. Rev. Microbiol. 3:753764.
62. Idnurm, A., and, J. Heitman. 2005. Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol. 3:e95.
63. Idnurm, A.,, F.J. Walton,, A. Floyd,, and J. Heitman. 2008. Identification of the sex genes in an early diverged fungus. Nature 451:193196.
64. Inada, K.,, Y. Morimoto,, T. Arima, Y. Murata,, and T. Kamada. 2001. The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics 157:133140.
65. James, T. Y.,, P. Srivilai,, U. Kues,, and R. Vilgalys. 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 172:18771891.
66. Kahmann, R.,, and J. Schirrawski. 2007. Mating in the smut fungi: from a to b to the downstream cascades, p. 377387. In J. Heitman,, J. W. Kronstad,, J. W. Taylor,, and L. A. Casselton (ed.), Sex in Fungi. ASM Press, Washington, DC.
67. Kamper, J.,, M. Reichmann,, T. Romeis, M. Bolker,, and R. Kahmann. 1995. Multiallelic recognition: nonselfdependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:7383.
68. Karos, M.,, Y.C. Chang,, C.M. McClelland,, D.L. Clarke,, J. Fu,, B. L. Wickes,, and K. J. Kwon-Chung. 2000. Mapping of the Cryptococcus neoformans MATα locus: presence of mating type-specific mitogen-activated protein kinase cascade homologs. J. Bacteriol. 182:62226227.
69. Kent, C. R., P. Ortiz-Bermudez, S. S. Giles, and, C. M. Hull. 2008. Formulation of a defined V8 medium for induction of sexual development of Cryptococcus neoformans. Appl. Environ. Microbiol. 74:62486253.
70. Kim, H., and, K. A. Borkovich. 2006. Pheromones are essential for male fertility and sufficient to direct chemo-tropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot. Cell 5:544554.
71. Kim, J.,, E. Bortz,, H. Zhong, T. Leeuw,, E. Leberer, A. K. Vershon,, and J. P. Hirsch. 2000. Localization and signaling of G(beta) subunit Ste4p are controlled by a-factor receptor and the a-specific protein Asg7p. Mol. Cell. Biol. 20:88268835.
72. Kim, J., A. Couve, and, J. P. Hirsch. 1999. Receptor inhibition of pheromone signaling is mediated by the Ste4p Gbeta subunit. Mol. Cell. Biol. 19:441449.
73. Klengel, T.,, W.J. Liang,, J. Chaloupka, C. Ruoff,, K. Schroppel,, J. R Naglik,, S.E. Eckert,, E. G Mogensen,, K. Haynes,, M. F Tuite,, L.R. Levin,, J. Buck,, and F. A. Muhlschlegel. 2005. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr. Biol. 15:20212026.
74. Konopka, J. B.,, S.M. Margarit, and, P. Dube. 1996. Mutation of Pro-258 in transmembrane domain 6 constitutively activates the G protein-coupled alpha-factor receptor. Proc. Natl. Acad. Sci. USA 93:67646769.
75. Kozubowski, L.,, S.C. Lee, and, J. Heitman. 2009. Signalling pathways in the pathogenesis of Cryptococcus. Cell Microbiol. 11:370380.
76. Kulkarni, R. D.,, M.R. Thon,, H. Pan,, and R. A. Dean. 2005. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol. 6:R24.
77. Kwon-Chung, K. J. 1975. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67:11971200.
78. Kwon-Chung, K. J. 1976. A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 68:943946.
79. Kwon-Chung, K. J. 1976. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68:821833.
80. Kwon-Chung, K. J. 1980. Nuclear genotypes of spore chains in Filobasidiella neoformans (Cryptococcus neoformans). Mycologia 72:418422.
81. Kwon-Chung, K. J. 1998. Filobasidiella Kwon-Chung, p. 656662. In C. P. Kurtzman, and J. W. Fell (ed.), The Yeasts: a Taxonomic Study, 4th ed. Elsevier Science, Amsterdam, The Netherlands.
82. Kwon-Chung, K. J., and, J. E. Bennett. 1978. Distribution of alpha and a mating types of Cryptococcus neoformans among natural and clinical isolates. Am. J. Epidemiol. 108:337340.
83. Kwon-Chung, K. J., J. E. Bennett, and, J. C. Rhodes. 1982. Taxonomic studies on Filobasidiella species and their anamorphs. Antonie Van Leeuwenhoek 48:2538.
84. Kwon-Chung, K. J.,, Y.C. Chang,, R. Bauer,, E. C Swann,, J. W. Taylor,, and R. Goel. 1995. The characteristics that differentiate Filobasidiella depauperata from Filobasidiella neoformans. Stud. Mycol. 38:6779.
85. Kwon-Chung, K. J., J. C. Edman, and, B. L. Wickes. 1992. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 60:602605.
86. Kwon-Chung, K. J., and, T. J. Popkin. 1976. Ultrastructure of septal complex in Filobasidiella neoformans (Cryptococcus neoformans). J. Bacteriol. 126:524528.
87. Kwon-Chung, K. J., and, A. Varma. 2006. Do major species concepts support one, two or more species within Cryptococcus neoformans? FEMS Yeast Res. 6:574587.
88. Ladds, G.,, K. Davis,, A. Das,, and J. Davey. 2005. A constitutively active GPCR retains its G protein specificity and the ability to form dimers. Mol. Microbiol. 55:482497.
89. Lee, S. C.,, N. Corradi, E. J. Byrnes,, 3rd, S. Torres-Martinez,, F. S Dietrich,, P. J. Keeling,, and J. Heitman. 2008. Microsporidia evolved from ancestral sexual fungi. Curr. Biol. 18:16751679.
90. Lengeler, K. B.,, R.C. Davidson,, C. D’Souza,, T. Harashima,, W. C Shen,, P. Wang,, X. Pan,, M. Waugh,, and J. Heitman. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746785.
91. Leonard, T. J., and, S. Dick. 1968. Chemical induction of haploid fruiting bodies in Schizophyllum commune. Proc. Natl. Acad. Sci. USA 59:745751.
92. Leslie, J. F., and, T. J. Leonard. 1984. Nuclear control of monokaryotic fruiting in Schizophyllum commune. Mycologia 76:760763.
93. Li, L.,, G. Shen,, Z.G. Zhang,, Y. L. Wang, J. K. Thompson,, and P. Wang. 2007. Canonical heterotrimeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol. Biol. Cell 18:42014209.
94. Lin, X. 2009. Cryptococcus neoformans: morphogenesis, infection, and evolution. Infect. Genet. Evol. 9:401416.
95. Lin, X., and, J. Heitman. 2005. Chlamydospore formation during hyphal growth in Cryptococcus neoformans. Eukaryot. Cell 4:17461754.
96. Lin, X.,, J.C. Huang,, T.G. Mitchell,, and J. Heitman. 2006. Virulence attributes and hyphal growth of C. neoformans are quantitative traits and the MATalpha allele enhances filamentation. PLoS Genet. 2:e187.
97. Lin, X.,, C.M. Hull, and, J. Heitman. 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:10171021.
98. Lin, X.,, J.C. Jackson,, M. Feretzaki, C. Xue,, and J. Heitman. 2010. Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and samesex mating in Cryptococcus neoformans. PLoS Genet. 6:e1000953.
99. Lin, X.,, A. Litvintseva,, K. Nielsen,, S. Patel,, Z. Kapadia,, A. Floyd,, T. G. Mitchell,, and J. Heitman. 2007. αADα hybrids of Cryptococcus neoformans: evidence of same sex mating in nature and hybrid fitness. PLoS Genet. 3:19751990.
100. Lin, X.,, S. Patel,, A.P. Litvintseva,, A. Floyd, T. G. Mitchell,, and J. Heitman. 2009. Diploids in the Cryptococcus neoformans serotype A population homozygous for the alpha mating type originate via unisexual mating. PLoS Pathog. 5:e1000283.
101. Liu, Y., Q. He, and, P. Cheng. 2003. Photoreception in Neurospora: a tale of two White Collar proteins. Cell. Mol. Life Sci. 60:21312138.
102. Lu, Y. K., K. H. Sun, and, W. C. Shen. 2005. Blue light negatively regulates the sexual filamentation via the Cwc1 and Cwc2 proteins in Cryptococcus neoformans. Mol. Microbiol. 56:480491.
103. Marra, R. E.,, J.C. Huang,, E. Fung,, K. Nielsen,, J. Heitman,, R. Vilgalys,, and T. G. Mitchell. 2004. A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167:619631.
104. Martin, F.,, A. Aerts,, D. Ahren,, A. Brun,, E.G. Danchin,, F. Duchaussoy,, J. Gibon,, A. Kohler,, E. Lindquist,, V. Pereda,, A. Salamov,, H. J Shapiro,, J. Wuyts,, D. Blaudez,, M. Buee,, P. Brokstein,, B. Canback,, D. Cohen,, P. E Courty,, P. M. Coutinho,, C. Delaruelle,, J. C Detter,, A. Deveau,, S. DiFazio,, S. Duplessis,, L. Fraissinet-Tachet,, E. Lucic,, P. Frey-Klett,, C. Fourrey,, I. Feussner,, G. Gay,, J. Grimwood,, P. J Hoegger,, P. Jain,, S. Kilaru,, J. Labbe,, Y. C Lin,, V. Legue,, F. Le Tacon,, R. Marmeisse,, D. Melayah,, B. Montanini,, M. Muratet,, U. Nehls,, H. Niculita-Hirzel,, M. P. Oudot-Le Secq,, M. Peter,, H. Quesneville,, B. Rajashekar,, M. Reich,, N. Rouhier,, J. Schmutz,, T. Yin,, M. Chalot,, B. Henrissat,, U. Kues,, S. Lucas,, Y. Van de Peer,, G. K Podila,, A. Polle,, P. J Pukkila,, P. M. Richardson,, P. Rouze,, I. R Sanders,, J. E. Stajich,, A. Tunlid,, G. Tuskan,, and I. V. Grigoriev. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:8892.
105. Miyake, H., K. Tanaka, and, T. Ishikawa. 1980. Basid-iospore formation in monokaryotic fruiting bodies of a mutant strain of Coprinus macrorhizus. Arch. Microbiol. 126:207211.
106. Mizushina, Y.,, L. Hanashima,, T. Yamaguchi,, M. Takemura,, F. Sugawara,, M. Saneyoshi,, A. Matsukage,, S. Yoshida,, and K. Sakaguchi. 1998. A mushroom fruiting body-inducing substance inhibits activities of replicative DNA polymerases. Biochem. Biophys. Res. Commun. 249:1722.
107. Mogensen, E. G.,, G. Janbon, J. Chaloupka,, C. Steeg-born,, M. S Fu,, F. Moyrand,, T. Klengel,, D. S Pearson,, M.A. Geeves,, J. Buck,, L. R. Levin,, and F. A. Muhlschlegel. 2006. Cryptococcus neoformans senses CO 2through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot. Cell 5:103111.
108. Moore, D. 1998. Fungal Morphogenesis. Cambridge University Press, Cambridge, United Kingdom.
109. Muller, H.,, C. Hennequin,, J. Gallaud, B. Dujon,, and C. Fairhead. 2008. The asexual yeast Candida glabrata maintains distinct a and alpha haploid mating types. Eukaryot. Cell 7:848858.
110. Murata, Y.,, M. Fujii,, M.E. Zolan,, and T. Kamada. 1998. Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 149:17531761.
111. Nguyen, V. Q., and, A. Sil. 2008. Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc. Natl. Acad. Sci. USA 105:48804885.
112. Nichols, C. B.,, J.A. Fraser, and, J. Heitman. 2004. PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating in Cryptococcus neoformans. Mol. Biol. Cell 15:44764489.
113. Niculita-Hirzel, H.,, J. Labbe,, A. Kohler, F. le Tacon,, F. Martin, I. R. Sanders,, and U. Kues. 2008. Gene organization of the mating type regions in the ectomycorrhizal fungus Laccaria bicolor reveals distinct evolution between the two mating type loci. New Phytol. 180:329342.
114. Nielsen, K.,, G.M. Cox,, P. Wang, D. L. Toffaletti,, J.R. Perfect,, and J. Heitman. 2003. Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and alpha isolates. Infect. Immun. 71:48314841.
115. Nielsen, K.,, A. L. De Obaldia, and, J. Heitman. 2007. Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot. Cell 6:949959.
116. Odom, A.,, S. Muir,, E. Lim, D. L. Toffaletti,, J. Perfect,, and J. Heitman. 1997. Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J. 16:25762589.
117. Oishi, K., I. Uno, and, T. Ishikawa. 1982. Timing of DNA replication during the meiotic process in monokaryotic basidiocarps of Coprinus macrorhizus. Arch. Microbiol. 132:372374.
118. Olive, L. S. 1968. An unusual heterobasidiomycete with tilletia-like basidia. J. Elisha Mitchell Sci. Soc. 84:261266.
119. Palmer, D. A.,, J.K. Thompson,, L. Li, A. Prat,, and P. Wang. 2006. Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J. Biol. Chem. 281:3259632605.
120. Paoletti, M.,, C. Rydholm,, E.U. Schwier,, M.J. Anderson,, G. Szakacs,, F. Lutzoni,, J. P Debeaupuis,, J.P. Latge,, D. W. Denning,, and P. S. Dyer. 2005. Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr. Biol. 15:12421248.
121. Poggeler, S., and, U. Kuck. 2001. Identification of transcriptionally expressed pheromone receptor genes in filamentous ascomycetes. Gene 280:917.
122. Prusty, R., P. Grisafi, and, G. R. Fink. 2004. The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:41534157.
123. Raju, N. B. 1978. Meiosis nuclear behaviour and ascospore formation in five homothallic species of Neurospora. Can. J. Bot. 56:754763.
124. Raju, N. B. 1980. Meiosis and ascospore genesis in Neurospora. Eur. J. Cell Biol. 23:208223.
125. Raju, N. B. 1992. Functional heterothallism resulting from homokaryotic conidia and ascospores in Neurospora tetrasperma. Mycol. Res. 96:103116.
126. Raju, N. B. 1992. Genetic control of the sexual cycle in Neurospora. Mycol. Res. 96:241262.
127. Raju, N. B., and, D. D. Perkins. 1994. Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Dev. Genet. 15:104118.
128. Ren, P.,, D.J. Springer,, M.J. Behr,, W. A. Samsonoff, S. Chaturvedi,, and V. Chaturvedi. 2006. Transcription factor STE12alpha has distinct roles in morphogenesis, virulence, and ecological fitness of the primary pathogenic yeast Cryptococcus gattii. Eukaryot. Cell 5:10651080.
129. Riquelme, M.,, M. P Challen,, L. A. Casselton, and, A. J. Brown. 2005. The origin of multiple B mating specificities in Coprinus cinereus. Genetics 170:11051119.
130. Rogers, A. L., K. J. Kwon-Chung, and, S. L. Flegler. 1980. A scanning electron microscope comparison of basidial structures in Filobasidiella neoformans and Filobasidiella bacillispora. Sabouraudia 18:8589.
131. Roth, A. F.,, B. Nelson,, C. Boone, and, N. G. Davis. 2000. Asg7p-Ste3p inhibition of pheromone signaling: regulation of the zygotic transition to vegetative growth. Mol. Cell. Biol. 20:88158825.
132. Rutherford, J. C.,, X. Lin,, K. Nielsen,, and J. Heitman. 2008. Amt2 permease is required to induce ammoniumresponsive invasive growth and mating in Cryptococcus neoformans. Eukaryot. Cell 7:237246.
133. Saul, N., M. Krockenberger, and, D. Carter. 2008. Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot. Cell 7:727734.
134. Scherer, M.,, K. Heimel,, V. Starke,, and J. Kamper. 2006. The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18:23882401.
135. Schubert, D.,, M. Raudaskoski,, N. Knabe,, and E. Kothe. 2006. Ras GTPase-activating protein Gap1 of the homobasidiomycete Schizophyllum commune regulates hyphal growth orientation and sexual development. Eukaryot. Cell 5:683695.
136. Schulz, B.,, F. Banuett,, M. Dahl, R. Schlesinger,, W. Schafer,, T. Martin,, I. Herskowitz,, and R. Kahmann. 1990. The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60:295306.
137. Seo, J. A., K. H. Han, and, J. H. Yu. 2004. The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol. Microbiol. 53:16111623.
138. Shadomy, H. J. 1970. Clamp connections in two strains of Cryptococcus neoformans. Spectrum Monograph Series 1:6772. Georgia State University, Atlanta, GA.
139. Shadomy, H. J., and, J. P. Utz. 1966. Preliminary studies on a hypha-forming mutant of Cryptococcus neoformans. Mycologia 58:383390.
140. Shapiro, R. S.,, P. Uppuluri, A. K. Zaas,, C. Collins,, H. Senn,, J. R Perfect,, J. Heitman,, and L. E. Cowen. 2009. Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr. Biol. 19:621629.
141. Shen, G.,, Y.L. Wang,, A. Whittington, L. Li,, and P. Wang. 2008. The RGS protein Crg2 regulates pheromone and cyclic AMP signaling in Cryptococcus neoformans. Eukaryot. Cell 7:15401548.
142. Shen, W. C.,, R.C. Davidson,, G.M. Cox,, and J. Heitman. 2002. Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans. Eukaryot. Cell 1:366377.
143. Shi, C.,, S. Kaminskyj,, S. Caldwell, and, M. C. Loewen. 2007. A role for a complex between activated G proteincoupled receptors in yeast cellular mating. Proc. Natl. Acad. Sci. USA 104:53955400.
144. Sia, R. A.,, K.B. Lengeler, and, J. Heitman. 2000. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet. Biol. 29:153163.
145. Stahl, U., and, K. Esser. 1976. Genetics of fruit body production in higher basidiomycetes. I. Monokaryotic fruiting and its correlation with dikaryotic fruiting in Polyporus ciliatus. Mol. Gen. Genet. 148:183197.
146. Staib, F. 1981. The perfect state of Cryptococcus neoformans, Filobasidiella neoformans, on pigeon manure filtrate agar. Zentralbl. Bakteriol. A 248:575578.
147. Staib, F., and, A. Blisse. 1982. Bird manure filtrate agar for the formation of the perfect state of Cryptococcus neoformans, Filobasidiella neoformans. A comparative study of the agars prepared from pigeon and canary manure. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 251:554562.
148. Stanton, B. C.,, S.S. Giles,, M. W. Staudt, E. K. Kruzel,, and C. M. Hull. 2010. Allelic exchange of pheromones and their receptors reprograms sexual identity in Cryptococcus neoformans. PLos Genet. 6:e1000860.
149. Stefan, C. J., M. C. Overton, and, K. J. Blumer. 1998. Mechanisms governing the activation and trafficking of yeast G protein-coupled receptors. Mol. Biol. Cell 9:885899.
150. Strickfaden, S. C., and, P. M. Pryciak. 2008. Distinct roles for two Galpha-Gbeta interfaces in cell polarity control by a yeast heterotrimeric G protein. Mol. Biol. Cell 19:181197.
151. Swamy, S., I. Uno, and, T. Ishikawa. 1984. Morphogenetic effects of mutations at the A and B incompatibility factors of Coprinus cinereus. J. Gen. Microbiol. 130:32193224.
152. Tesmer, J. J.,, D.M. Berman,, A.G. Gilman,, and S. R. Sprang. 1997. Structure of RGS4 bound to AlF4-activated G(i alpha1): stabilization of the transition state for GTP hydrolysis. Cell 89:251261.
153. Torres-Guererro, H., and, J. C. Edman. 1994. Melanindeficient mutants of Cryptococcus neoformans. J. Med. Vet. Mycol. 32:303313.
154. Tscharke, R. L.,, M. Lazera, Y. C. Chang,, B.L. Wickes,, and K. J. Kwon-Chung. 2003. Haploid fruiting in Cryptococcus neoformans is not mating type alpha-specific. Fungal Genet. Biol. 39:230237.
155. Uno, I., and, T. Ishikawa. 1971. Chemical and genetical control of induction of monokaryotic fruiting bodies in Coprinus macrorhizus. Mol. Gen. Genet. 113:229239.
156. Uno, I., and, T. Ishikawa. 1973. Purification and identification of the fruiting-inducing substances in Coprinus macrorhizus. J. Bacteriol. 113:12401248.
157. Urayama, T. 1969. Stimulative effect of extracts from fruit bodies of Agaricus bisporus and some other hymenomycetes on primordia formation in Marasmius sp. Trans. Mycol. Soc. Jpn. 10:7378.
158. Velagapudi, R.,, Y.P. Hsueh,, S. Geunes-Boyer, J. R. Wright,, and J. Heitman. 2009. Spores as infectious propagules of Cryptococcus neoformans. Infect. Immun. 77:43454355.
159. Verrinder-Gibbins, A. M., and, B. C. Lu. 1984. Induction of normal fruiting on originally monokaryotic cultures of Coprinus cinereus. Trans. Br. Mycol. Soc. 82:331335.
160. Walton, F. J.,, A. Idnurm, and, J. Heitman. 2005. Novel gene functions required for melanization of the human pathogen Cryptococcus neoformans. Mol. Microbiol. 57:13811396.
161. Wang, P.,, J. Cutler,, J. King,, and D. Palmer. 2004. Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryot. Cell 3:10281035.
162. Wang, P.,, C.B. Nichols,, K.B. Lengeler,, M.E. Cardenas,, G. M Cox,, J. R. Perfect,, and J. Heitman. 2002. Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot. Cell 1:257272.
163. Wang, P.,, J.R. Perfect, and, J. Heitman. 2000. The G-protein beta subunit Gpb1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell. Biol. 20:352362.
164. Weber, M.,, V. Salo,, M. Uuskallio,, and M. Raudaskoski. 2005. Ectopic expression of a constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genet. Biol. 42:624637.
165. Webster, R. H., and, A. Sil. 2008. Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc. Natl. Acad. Sci. USA 105:1457314578.
166. Wickes, B. L., U. Edman, and, J. C. Edman. 1997. The Cryptococcus neoformans STE12α gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol. Microbiol. 26:951960.
167. Wickes, B. L.,, M.E. Mayorga,, U. Edman,, and J. C. Edman. 1996. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type. Proc. Natl. Acad. Sci. USA 93:73277331.
168. Xue, C.,, Y.S. Bahn,, G.M. Cox,, and J. Heitman. 2006. G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol. Biol. Cell 17:667679.
169. Xue, C.,, Y.P. Hsueh,, L. Chen,, and J. Heitman. 2008. The RGS protein Crg2 regulates both pheromone and cAMP signalling in Cryptococcus neoformans. Mol. Microbiol. 70:379395.
170. Xue, C.,, Y.P. Hsueh, and, J. Heitman. 2008. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol. Rev. 32:10101032.
171. Xue, C.,, Y. Tada,, X. Dong,, and J. Heitman. 2007. The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1:263273.
172. Yeh, Y. L.,, Y.S. Lin,, B.J. Su,, and W. C. Shen. 2009. A screening for suppressor mutants reveals components involved in the blue light-inhibited sexual filamentation in Cryptococcus neoformans. Fungal Genet. Biol. 46:4254.
173. Yi, S.,, N. Sahni,, K.J. Daniels,, C. Pujol, T. Srikantha,, and D. R. Soll. 2008. The same receptor, G protein, and mitogen-activated protein kinase pathway activate different downstream regulators in the alternative white and opaque pheromone responses of Candida albicans. Mol. Biol. Cell 19:957970.
174. Young, L. Y.,, M.C. Lorenz, and, J. Heitman. 2000. A STE12 homolog is required for mating but dispensable for filamentation in Candida lusitaniae. Genetics 155:1729.
175. Yue, C.,, L. M. Cavallo,, J. A. Alspaugh,, P. Wang,, G. M. Cox,, J. R. Perfect,, and J. Heitman. 1999. The STE12α homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 153:16011615.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error