Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism

Xiaorong Lin; Joseph Heitman

doi:10.1128/9781555815837.ch3

Chapter 3 : Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Departments of Molecular Genetics and Microbiology, Pharmacology and Cancer Biology, and Medicine, Duke University Medical Center, Durham, NC 27710; 2: Departments of Molecular Genetics and Microbiology, Pharmacology and Cancer Biology, and Medicine, Duke University Medical Center, Durham, NC 27710

Content Type: Monograph

Publication Year: 2007

Category: Fungi and Fungal Pathogenesis

Book DOI: 10.1128/9781555815837

Chapter DOI: 10.1128/9781555815837.ch3

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

Preview this chapter:

Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815837/9781555814212_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555815837/9781555814212_Chap03-2.gif

Abstract:

Sexual systems are classified into heterothallism or homothallism in fungi. This chapter focuses on examples of homothallic fungi and how their sexuality is governed. Conversions between heterothallic and homothallic sexual cycles are common evolutionary transitions in fungi, and whether homothallism evolved from heterothallism or vice versa is a controversial topic, and there is evidence supporting both hypotheses. The structural analyses of MAT sequences from homothallic and heterothallic Cochliobolus species support the hypothesis that heterothallism is the ancestral state in this genus. This unique arrangement of the Aspergillus nidulans MAT locus led to the proposal that homothallism is the ancestral state and that a transition from homothallism to heterothallism could have occurred in A. oryzae and A. fumigatus by gene loss, although neither species has a defined sexual cycle. Homothallic species may originate from heterothallic predecessors, and the homothallic lifestyle may have a selective advantage under certain ecological pressures. This hypothesis is consistent with the repeated occurrence of homothallism within numerous genera and the fact that many heterothallic fungi achieve homothallism in the form of pseudohomothallism by mating-type switching or packaging two compatible nuclei into one spore. Homothallic individuals contain all of the necessary genetic information for full sexual expression.

Citation: Lin X, Heitman J. 2007. Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism, p 35-57. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch3

Highlighted Text: Show | Hide

Full text loading...

Figures

Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815837.ch03-1,webId=/content/author/10.1128/9781555815837.ch03-1,properties={foaf_givenname=Xiaorong, foaf_name=Xiaorong Lin, foaf_surname=Lin, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815837.ch03-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815837.ch03-2,webId=/content/author/10.1128/9781555815837.ch03-2,properties={foaf_givenname=Joseph, foaf_name=Joseph Heitman, foaf_surname=Heitman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815837.ch03-aff2]]}]]

/content/10.1128/9781555815837.ch03.ch03fig01

Figure 3.1

Heterothallic sexual reproduction in ascomycetes (upper row) and basidiomycetes (bottom row) shares several conserved features. A cell fusion event creates a dikaryotic state, and then, nuclear fusion occurs followed by meiosis and sporulation. The small circles represent nuclei. The solid and open circles indicate nuclei from different individuals.

10.1128/9781555815837/f0036-01_thmb.gif

10.1128/9781555815837/f0036-01.gif

Figure 3.1

/content/10.1128/9781555815837.ch03.ch03fig02

Figure 3.2

Mating-type switching in Saccharomyces cerevisiae. The mother cell (depicted as a) undergoes mating-type switching to α and then mates with the daughter cell (a) to create a heterozygous diploid (a/α). This diploid cell can either amplify by mitosis through budding (not depicted) under rich media conditions or, in response to nitrogen limitation and nonfermentable carbon source, undergo meiosis to produce four meiotic ascospores with two a cells and two α cells. Solid and open circles indicate nuclei of a and α mating type. Only the shaded locus (MAT) is expressed. The thickness of the arrow represents the efficiency of the switching event. Arrows indicate the direction of the switching event.

10.1128/9781555815837/f0037-01_thmb.gif

10.1128/9781555815837/f0037-01.gif

Figure 3.2

/content/10.1128/9781555815837.ch03.ch03fig03

Figure 3.3

Mating-type switching in Schizosaccharomyces pombe. The mother cell (P) undergoes a mating-type switch to M and then mates with the daughter cell (P) to create a heterozygous diploid cell (P/M), which undergoes meiosis immediately to produce four meiotic ascospores with two P cells and two M cells. Solid and open small circles indicate nuclei of P and M mating type. H1 and H2 are conserved flanking sequences for all three cassettes. H3 is a conserved element of the mat2P and mat3M silent cassettes. These conserved sequences are involved in regulation of mating-type expression and switching (for details, see the chapter by Nielsen and Egel [chapter 8]). Only the shaded locus (mat1) is expressed. The thickness of the arrow represents the efficiency of the switching event. Arrows indicate the direction of the switching event.

10.1128/9781555815837/f0039-01_thmb.gif

10.1128/9781555815837/f0039-01.gif

Figure 3.3

/content/10.1128/9781555815837.ch03.ch03fig04

Figure 3.4

One form of pseudohomothallism involves packaging two nuclei of compatible mating type into a single spore. The dikaryon contains two nuclei of different but compatible mating types (for example, MAT-1 and MAT-2). After nuclear fusion in the basidium/ascus, meiosis occurs and four nuclei are produced. Two nuclei of each mating type are packaged into one spore, which gives rise to a dikaryon competent for sexual reproduction after germination.

10.1128/9781555815837/f0040-01_thmb.gif

10.1128/9781555815837/f0040-01.gif

Figure 3.4

/content/10.1128/9781555815837.ch03.ch03fig05

Figure 3.5

Three molecular mechanisms of primary homothallism. The homokaryotic hyphae (a monokaryon in this figure) can undergo nuclear fusion, meiosis, and sporulation in the absence of a partner. The MAT structure in these homothallic fungi can be as follows: two fused idiomorphs are present in a single genome (I); two idiomorphs are present in a single genome but located at different genomic regions (II); and only MAT-1 is present, and MAT-2 is absent (III).

10.1128/9781555815837/f0041-01_thmb.gif

10.1128/9781555815837/f0041-01.gif

Figure 3.5

/content/10.1128/9781555815837.ch03.ch03fig06

Figure 3.6

Aspergillus MAT structures and their evolution. Arrangement of the MAT idiomorphs and their flanking genes for A. nidulans, N. fischeri, A. fumigatus, and A. oryzae are shown. Homologous coding regions are color coded and indicated in the corresponding boxes. Arrows indicate the direction of expression. Hypotheses regarding the transition between homothallism and heterothallism in this genus are depicted. See the text and the chapters by Butler (chapter 1) and Dyer (chapter 7) for details.

10.1128/9781555815837/f0043-01_thmb.gif

10.1128/9781555815837/f0043-01.gif

Figure 3.6

/content/10.1128/9781555815837.ch03.ch03fig07

Figure 3.7

The sexual cycle of Cryptococcus neoformans. During mating (the heterothallic life cycle), a and α yeast cells undergo cell-cell fusion and produce dikaryotic hyphae. At the stage of basidium development, the two parental nuclei fuse and undergo meiosis to produce four meiotic products that form chains of basidiospores by repeated mitosis and budding. During monokaryotic fruiting (the homothallic life cycle), cells of one mating type, e.g., α cells, become diploid α/α cells, either by endoreplication or by cell fusion followed by nuclear fusion between two α cells. At the stage of basidium development, meiosis occurs and haploid basidiospores of one mating type are produced in four chains.

10.1128/9781555815837/f0048-01_thmb.gif

10.1128/9781555815837/f0048-01.gif

Figure 3.7

References

/content/book/10.1128/9781555815837.ch03

1. Arcangioli, B., and, R. de Lahondes. 2000. Fission yeast switches mating type by a replication-recombination coupled process. EMBO J. 19: 1389– 1396.

2. Arita, I. 1978. Pholiota nameko, p. 475–496. In S. T. Chang and, W. A. Hayes (ed.), The Biology and Cultivation of Edible Mushrooms. Academic Press, New York, NY.

3. Arnaise, S.,, D. Zickler, and, N. L. Glass. 1993. Heterologous expression of mating-type genes in filamentous fungi. Proc. Natl. Acad. Sci. USA 90: 6616– 6620.

4. Barnett, J. A.,, R. W. Payne, and, D. Yarrow. 2000. Yeasts: Characteristics and Identification, 3rd ed. Cambridge University Press, Cambridge, United Kingdom.

5. Baroiller, J. F., and, H. D’Cotta. 2001. Environment and sex determination in farmed fish. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130: 399– 409.

6. Beatty, N. P.,, M. L. Smith, and, N. L. Glass. 1994. Molecular characterization of mating-type loci in selected homothallic species of Neurospora, Gelasinospora and Anixiella. Mycol. Res. 98: 1309- 1316.

7. Biggs, R. 1938. Cultural studies in the Thelephoraceae and related fungi. Mycologia 30: 64– 78.

8. Bressan,, D. A., J. Vazquez, and, J. E. Haber. 2004. Mating-type-dependent constraints on the mobility of the left arm of yeast chromosome III. J. Cell Biol. 164: 361– 371.

9. Butler, G.,, C. Kenny,, A. Fagan,, C. Kurischko,, C. Gaillardin, and, K. H. Wolfe. 2004. Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc. Natl. Acad. Sci. USA 101: 1632– 1637.

10. Callac, P.,, I. J. de Haut,, M. Imbernon,, J. Guinberteau,, C. Desmerger, and, I. Theochari. 2003. A novel homothallic variety of Agaricus bisporus comprises rare tetrasporic isolates from Europe. Mycologia 95: 222– 231.

11. Callac, P.,, S. Hocquart,, M. Imbernon,, C. Desmerger, and, J. M. Olivier. 1998. Bsn-t alleles from French field strains of Agaricus bisporus. Appl. Environ. Microbiol. 64: 2105– 2110.

12. Callac, P.,, M. Imbernon,, J. Guinberteau,, L. Pirobe,, S. Granit, and, J. M. Olivier. 2000. Discovery of a wild Mediterranean population of Agaricus bisporus, and its usefulness for breeding work. Mushroom Sci. 15: 245– 252.

13. Callac, P.,, C. Spataro,, A. Caille, and, M. Imbernon. 2006. Evidence for outcrossing via the Buller phenomenon in a substrate simultaneously inoculated with spores and mycelium of Agaricus bisporus. Appl. Environ. Microbiol. 72: 2366– 2372.

14. Callac, P.,, I. Theochari, and, R. W. Kerrigan. 2002. The germplasm of Agaricus bisporus: main results after ten years of collecting in France, in Greece, and in North America. Acta Hortic. 579: 49– 55.

15. Calvo-Bado, L.,, R. Noble,, M. Challen,, A. Dobrovin Pennington, and, T. Elliott. 2000. Sexuality and genetic identity in the Agaricus section Arvenses. Appl. Environ. Microbiol. 66: 728– 734.

16. Casselton, L. A., and, U. Kues. 1994. Mating-type genes in homobasidiomycetes, p. 307–321. In J. W. Wessels and, F. Meinhardt (ed.), The Mycota, vol. 1. Springer-Verlag, Berlin, Germany.

17. Casselton, L. A., and, N. S. Olesnicky. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62: 55– 70.

18. Challen, M. P.,, R. W. Kerrigan, and, P. Callac. 2003. A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae. Mycologia 95: 61– 73.

19. Cisar, C. R., and, D. O. TeBeest. 1999. Mating system of the filamentous ascomycete, Glomerella cingulata. Curr. Genet. 35: 127– 133.

20. Coppin, E.,, R. Debuchy,, S. Arnaise, and, M. Picard. 1997. Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol. Biol. Rev. 61: 411– 428.

21. Cozijnsen, A. J., and, B. J. Howlett. 2003. Characterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans. Curr. Genet. 43: 351– 357.

22. Cushion, M. T. 1998. Taxonomy, genetic organization, and life cycle of Pneumocystis carinii. Semin. Respir. Infect. 13: 304– 312.

23. Cushion, M. T., and, A. G. Smulian. 2001. The Pneumocystis genome project: update and issues. J. Eukaryot. Microbiol. Suppl: 182S– 183S.

24. Dalgaard, J. Z., and, A. J. Klar. 1999. Orientation of DNA replication establishes mating-type switching pattern in S. pombe. Nature 400: 181– 184.

25. Day, P. R. 1963. Mutations of the A mating type factor in Coprinus lagopus. Genet. Res. Camb. 4: 55– 64.

26. Debuchy,, R., and B. G. Turgeon. 2006. Mating-type structure, evolution, and function in euascomycetes, p. 293–323. In U. Kües and, R. Fischer (ed.), Growth, Differentiation and Sexuality, vol. I. Springer-Verlag, Berlin, Germany.

27. de Hoog, G. S.,, C. P. Kurtzman,, H. J. Phaff, and, M. W. Miller. 2000. Eremothecium borzi emend. Kurtzman, p. 201–208. In C. P. Kurtzman and, J. W. Fell (ed.), The Yeasts: a Taxonomic Study. Elsevier, Amsterdam, The Netherlands.

28. Dietrich, F. S.,, S. Voegeli,, S. Brachat,, A. Lerch,, K. Gates,, S. Steiner,, C. Mohr,, R. Pohlmann,, P. Luedi,, S. Choi,, R. A. Wing,, A. Flavier,, T. D. Gaffney, and, P. Philippsen. 2004. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304: 304– 307.

29. Dyer, P. S.,, M. Paoletti, and, D. B. Archer. 2003. Genomics reveals sexual secrets of Aspergillus. Microbiology 149: 2301– 2303.

30. Eileen Kennedy, M., and, J. H. Burnett. 1956. Amphithallism in fungi. Nature 177: 882– 883.

31. Elliott, T. J. 1985. Developmental genetics—from spore to sporephore, p. 451–465. In D. Moore,, L. A. Casselton,, D. A. Wood, and, J. C. Frankland (ed.), Developmental Biology of Higher Fungi. Cambridge University Press, Cambridge, United Kingdom.

32. Erke, K. H. 1976. Light microscopy of basidia, basidiospores, and nuclei in spores and hyphae of Filobasidiella neoformans ( Cryptococcus neoformans). J. Bacteriol. 128: 445– 455.

33. Esser, K., and, F. Meinhardt. 1977. A common genetic control of dikaryotic and monokaryotic fruiting in the basidiomycete Agrocybe aegerita. Mol. Gen. Genet. 155: 113– 115.

34. Esser, K.,, F. Saleh, and, F. Meinhardt. 1979. Genetics of fruit body production in higher basidiomycetes. 2. Monokaryotic and dikaryotic fruiting in Schizophyllum commune. Curr. Genet. 1: 85– 88.

35. Esser, K., and, J. Straub. 1958. Genetic studies on Sordaria macrospora Auersw., compensation and induction in gene-dependent developmental defects. Z. Vererbungsl. 89: 729– 746.

36. Fabre, E.,, H. Muller,, P. Therizols,, I. Lafontaine,, B. Dujon, and, C. Fairhead. 2005. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol. Biol. Evol. 22: 856– 873.

37. Fields, W. G. 1970. An introduction to the genus Sordaria. Neurospora Newsl. 16: 14– 17.

38. Fowler,, T. J., S. M. DeSimone,, M. F. Mitton,, J. Kurjan, and, C. A. Raper. 1999. Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol. Biol. Cell 10: 2559– 2572.

39. 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.

40. Frazer, H. L. 1944. Observations on the method of transmission of internal boll disease of cotton by the cotton stainer-bug. Ann. Appl. Biol. 21: 271– 290.

41. Frisvad,, J. C., and R. A. Samson. 1990. Chemotaxonomy and morphology of Aspergillus fumigatus and related taxa, p. 201–208. In R. A. Samson and, J. I. Pitt (ed.), Modern Concepts in Penicillium and Aspergillus Classification. Plenum Press, New York, NY.

42. Galagan, J. E.,, S. E. Calvo,, C. Cuomo,, L. J. Ma,, J. R. Wortman,, S. Batzoglou,, S. I. Lee,, M. Basturkmen,, C. C. Spevak,, J. Clutterbuck,, V. Kapitonov,, J. Jurka,, C. Scazzocchio,, M. Farman,, J. Butler,, S. Purcell,, S. Harris,, G. H. Braus,, O. Draht,, S. Busch,, C. D’Enfert,, C. Bouchier,, G. H. Goldman,, D. Bell-Pedersen,, S. Griffiths-Jones,, J. H. Doonan,, J. Yu,, K. Vienken,, A. Pain,, M. Freitag,, E. U. Selker,, D. B. Archer,, M. A. Penalva,, B. R. Oakley,, M. Momany,, T. Tanaka,, T. Kumagai,, K. Asai,, M. Machida,, W. C. Nierman,, D. W. Denning,, M. Caddick,, M. Hynes,, M. Paoletti,, R. Fischer,, B. Miller,, P. Dyer,, M. S. Sachs,, S. A. Osmani, and, B. W. Birren. 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105– 1115.

43. Geiser, D. M.,, W. E. Timberlake, and, M. L. Arnold. 1996. Loss of meiosis in Aspergillus. Mol. Biol. Evol. 13: 809– 817.

44. Ginns, J., and, D. W. Malloch. 2003. Filobasidiella depauperata (Tremellales): haustorial branches and parasitism of Verticillium lecani. Mycol. Prog. 2: 137– 140.

45. Giraud, T. 2004. Patterns of within population dispersal and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia. Heredity 93: 559– 565.

46. Glass,, N. L., J. Grotelueschen, and, R. L. Metzenberg. 1990. Neurospora crassa A mating-type region. Proc. Natl. Acad. Sci. USA 87: 4912– 4916.

47. Glass, N. L.,, R. L. Metzenberg, and, N. B. Raju. 1990. Homothallic Sordariaceae from nature: the absence of strains containing only the a mating-type sequence. Exp. Mycol. 14: 274– 289.

48. Glass, N. L., and, M. L. Smith. 1994. Structure and function of a mating-type gene from the homothallic species Neurospora africana. Mol. Gen. Genet. 244: 401– 409.

49. Glass, N. L.,, S. J. Vollmer,, C. Staben,, J. Grotelueschen,, R. L. Metzenberg, and, C. Yanofsky. 1988. DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science 241: 570– 573.

50. Griffiths, A. J. F. 1982. Null mutants of A and a mating type alleles of Neurospora crassa. Can. J. Genet. Cytol. 24: 167– 176.

51. Griffiths,, A. J. F., and A. M. Delange. 1978. Mutations of the a mating type in Neurospora crassa. Genetics 88: 239– 254.

52. 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 Leeuwenhoek 63: 175– 189.

53. Haber, J. E.,, L. Rowe, and, D. T. Rogers. 1981. Transposition of yeast mating-type genes from two translocations of the left arm of chromosome III. Mol. Cell. Biol. 1: 1106– 1119.

54. Han, K. H.,, J. A. Seo, and, J. H. Yu. 2004. A putative G protein-coupled receptor negatively controls sexual development in Aspergillus nidulans. Mol. Microbiol. 51: 1333– 1345.

55. Hanna, W. F. 1928. Sexual stability in monosporous mycelia of Coprinus lagopus. Ann. Bot. 42: 379– 388.

56. Harrington,, T. C., and D. L. McNew. 1997. Self-fertility and uni-directional mating-type switching in Ceratocystis coerulescens, a filamentous ascomycete. Curr. Genet. 32: 52– 59.

57. Heitman, J. 2006. Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 16: R711– R725.

58. Herman,, A., and H. Roman. 1966. Allele specific determinants of homothallism in Saccharomyces lactis. Genetics 53: 727– 740.

59. Herskowitz, I. 1988. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52: 536– 553.

60. Herskowitz,, I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342: 749– 757.

61. Herskowitz, I., and, Y. Oshima. 1981. Control of cell type in Saccharomyces cerevisiae: mating type and mating-type interconversion, p. 181–209. 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, Cold Spring Harbor, NY.

62. Herskowitz, I.,, J. Rine, and, J. Strathern. 1991. Mating-type determination and mating-type interconversion in Saccharomyces cerevisiae, p. 583–656. In J. R. Broach,, J. R. Pringle, and, E. W. Jones (ed.), The Molecular and Cellular Biology of the Yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

63. Hicks, J.,, J. N. Strathern, and, A. J. Klar. 1979. Transposable mating type genes in Saccharomyces cerevisiae. Nature 282: 478– 483.

64. Hiscock, S. J., and, U. Kües. 1999. Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int. Rev. Cytol. 193: 165– 295.

65. Hoffmann, B.,, S. E. Eckert,, S. Krappmann, and, G. H. Braus. 2001. Sexual diploids of Aspergillus nidulans do not form by random fusion of nuclei in the heterokaryon. Genetics 157: 141– 147.

66. Hood, M. E. 2002. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160: 457– 461.

67. Hood,, M. E., J. Antonovics, and, B. Koskella. 2004. Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms. Genetics 168: 141– 146.

68. Houston, P. L., and, J. R. Broach. 2006. The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet. 2: e98.

69. Hull, C. M.,, M. J. Boily, and, J. Heitman. 2005. Sexspecific homeodomain proteins Sxi1alpha and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot. Cell 4: 526– 535.

70. 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: 3046– 3060.

71. Hull, C. M., and, J. Heitman. 2002. Genetics of Cryptococcus neoformans. Annu. Rev. Genet. 36: 557– 615.

72. Imbernon, M.,, P. Callac,, P. Gasqui,, R. W. Kerrigan, and, J. Velcko. 1996. BSN, the primary determinant of basidial spore number and reproductive mode in Agaricus bisporus, maps to chromosome I. Mycologia 88: 749– 761.

73. Imbernon, M.,, P. Callac,, S. Granit, and, L. Pirobe. 1995. Allelic polymorphism at the mating type locus in Agaricus bisporus var. burnettii, and confirmation of the dominance of its tetrasporic trait. Mushroom Sci. 14: 11– 19.

74. Inderbitzin, P.,, J. Harkness,, B. G. Turgeon, and, M. L. Berbee. 2005. Lateral transfer of mating system in Stemphylium. Proc. Natl. Acad. Sci. USA 102: 11390– 11395.

75. James, S. A.,, M. D. Collins, and, I. N. Roberts. 1994. The genetic relationship of Lodderomyces elongisporus to other ascomycete yeast species as revealed by small-subunit rRNA gene sequences. Lett. Appl. Microbiol. 19: 308– 311.

76. Johnson, A. D. 1995. Molecular mechanisms of cell-type determination in budding yeast. Curr. Opin. Genet. Dev. 5: 552– 558.

77. Johnston,, J. R., C. Baccari, and, R. K. Mortimer. 2000. Genotypic characterization of strains of commercial wine yeasts by tetrad analysis. Res. Microbiol. 151: 583– 590.

78. Kaykov, A., and, B. Arcangioli. 2004. A programmed strand-specific and modified nick in S. pombe constitutes a novel type of chromosomal imprint. Curr. Biol. 14: 1924– 1928.

79. Kerrigan, R. W.,, M. Imbernon,, P. Callac,, C. Billette, and, J. M. Olivier. 1994. The heterothallic life cycle of Agaricus bisporus var. burnettii, and the inheritance of its tetrasporic trait. Exp. Mycol. 18: 193– 210.

80. Kerrigan, R. W.,, J. C. Royer,, L. M. Baller,, Y. Kohli,, P. A. Horgen, and, J. B. Anderson. 1993. Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics 133: 225– 236.

81. Klar, A. J.,, J. B. Hicks, and, J. N. Strathern. 1982. Directionality of yeast mating-type interconversion. Cell 28: 551– 561.

82. Kohn, L. M. 2005. Mechanisms of fungal speciation. Annu. Rev. Phytopathol. 43: 279– 308.

83. Koltin,, Y., J. Stamberg, and, P. A. Lemke. 1972. Genetic structure and evolution of the incompatibility factors in higher fungi. Bacteriol. Rev. 36: 156– 171.

84. Koopsman, A. 1977. A cytological study of Nematospora coryli Pegl. Genetica 47: 187– 195.

85. Kües,, U., and Y. Liu. 2000. Fruiting body production in Basidiomycetes. Appl. Microbiol. Biotechnol. 54: 141– 152.

86. Kurtzman, C. P. 2000. Lodderomyces van der Walt, p. 254–255. In C. P. Kurtzman and, J. W. Fell (ed.), The Yeasts: a Taxonomic Study, 4th ed. Elsevier, Amsterdam, The Netherlands.

87. Kwon-Chung, K. J. 1975. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67: 1197– 1200.

88. Kwon-Chung, K. J. 1976. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68: 821– 833.

89. Kwon-Chung, K. J. 1977. Heterothallism vs. self-fertile isolates of Filobasidiella neoforms ( Cryptococcus neoformans). Proc. 4th International Conference on Mycoses. 356: 204– 213. Pan American Health Organization, Washington, DC.

90. 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: 337– 340.

91. 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: 67– 79.

92. Labarere, J., and, T. Noel. 1992. Mating type switching in the tetrapolar basidiomycete Agrocybe aegerita. Genetics 131: 307– 319.

93. Lee, J.,, T. Lee,, Y. W. Lee,, S. H. Yun, and, B. G. Turgeon. 2003. Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol. Microbiol. 50: 145– 152.

94. Lemke, P. A. 1969. A reevaluation of homothallism, heterothallism and the species concept in Sistotrema brinkmanni. Mycologia 60: 57– 76.

95. Lengeler, K. B.,, D. S. Fox,, J. A. Fraser,, A. Allen,, K. Forrester,, F. S. Dietrich, and, J. Heitman. 2002. Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot. Cell 1: 704– 718.

96. Leonard, T. J., and, S. Dick. 1968. Chemical induction of haploid fruiting bodies in Schizophyllum commune. Proc. Natl. Acad. Sci. USA 59: 745– 751.

97. Leslie, J. F., and, T. J. Leonard. 1979. Monokaryotic fruiting in Schizophyllum commune: genetic control of the response to mechanical injury. Mol. Gen. Genet. 175: 5– 12.

98. Leslie, J. F., and, T. J. Leonard. 1980. Monokaryotic fruiting in Schizophyllum commune: survey of a population from Wisconsin. Am. Midl. Nat. 103: 367– 374.

99. Leslie, J. F., and, T. J. Leonard. 1984. Nuclear control of monokaryotic fruiting in Schizophyllum commune. Mycologia 76: 760– 763.

100. Leslie, J. F., and, T. J. Leonard. 1979. Three independent genetic systems that control initiation of a fungal fruiting body. Mol. Gen. Genet. 175: 257– 260.

101. Lin, X.,, J. C. Huang,, T. G. Mitchell, and, J. Heitman. 2006. Virulence attributes and hyphal growth of Cryptococcus neoformans are quantitative traits and the MAT α allele enhances filamentation. PLoS Genet. 2: e187, 1– 14.

102. Lin, X.,, C. M. Hull, and, J. Heitman. 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434: 1017– 1021.

103. Mainwaring, H. R., and, I. M. Wilson. 1968. The life cycle and cytology of an apomictic Podospora. Trans. Br. Mycol. Soc. 51: 663– 677.

104. Marra, R. E.,, P. Cortesi,, M. Bissegger, and, M. G. Milgroom. 2004. Mixed mating in natural populations of the chestnut blight fungus, Cryphonectria parasitica. Heredity 93: 189– 195.

105. 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: 619– 631.

106. Marra, R. E., and, M. G. Milgroom. 2001. The mating system of the fungus Cryphonectria parasitica: selfing and self-incompatibility. Heredity 86: 134– 143.

107. Martinez-Carrera, D.,, J. F. Smith,, M. P. Challen,, T. J. Elliott, and, C. F. Thurston. 1995. Homokaryotic fruiting in Agaricus bitorquis: a new approach. Mushroom Sci. 14: 29– 36.

108. Matsumoto, Y., and, Y. Yoshida. 1984. Sporogony in Pneumocystis carinii: synaptonemal complexes and meiotic nuclear divisions observed in precysts. J. Protozool. 31: 420– 428.

109. McCusker, J. H. 2006. Saccharomyces cerevisiae: an emerging and model pathogenic fungus, p. 245–259. In J. Heitman,, S. G. Filler,, J. E. Edwards, and, A. P. Mitchell (ed.), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC.

110. Meinhardt, F., and, K. Esser. 1981. Genetic studies of the basidiomycete Agrocybe aegerita. 2. Genetic control of fruit body formation and its practical implications. Theor. Appl. Genet. 60: 265– 268.

111. Meinhardt, F., and, J. F. Leslie. 1982. Mating types of Agrocybe aegerita. Curr. Genet. 5: 65– 68.

112. Metzenberg, R. L., and, N. L. Glass. 1990. Mating type and mating strategies in Neurospora. Bioessays 12: 53– 59.

113. Mitchell, A. P., and, I. Herskowitz. 1986. Activation of meiosis and sporulation by repression of the RME1 product in yeast. Nature 319: 738– 742.

114. Miyake, H.,, K. Tanaka, and, T. Ishikawa. 1980. Basidiospore formation in monokaryotic fruiting bodies of a mutant strain of Coprinus macrorhizus. Arch. Microbiol. 126: 207– 211.

115. Mizushina, Y.,, L. Hanashima,, T. Yamaguchi,, M. Take-mura,, 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: 17– 22.

116. Moore, D. 1998. Fungal Morphogenesis. Cambridge University Press, Cambridge, United Kingdom.

117. Moore, T. D., and, J. C. Edman. 1993. The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol. Cell. Biol. 13: 1962– 1970.

118. Mortimer, R. K.,, P. Romano,, G. Suzzi, and, M. Polsinelli. 1994. Genome renewal: a new phenomenon revealed from a genetic study of 43 strains of Saccharomyces cerevisiae derived from natural fermentation of grape musts. Yeast 10: 1543– 1552.

119. 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: 1753– 1761.

120. Nasmyth, K. A., and, K. Tatchell. 1980. The structure of transposable yeast mating type loci. Cell 19: 753– 764.

121. Nauta, M. J., and, R. F. Hoekstra. 1992. Evolution of reproductive systems in filamentous ascomycetes. II. Evolution of hermaphroditism and other reproductive strategies. Heredity 68: 537– 546.

122. Neuhauser, K. S., and, R. L. Gilbertson. 1971. Some aspects of bipolar heterothallism in Fomes cajanderi. Mycologia 63: 722– 735.

123. Ngugi, H. K., and, H. Scherm. 2006. Mimicry in plantparasitic fungi. FEMS Microbiol. Lett. 257: 171– 176.

124. 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: 4476– 4489.

125. 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: 372– 374.

126. O’Shea, S. F.,, P. T. Chaure,, J. R. Halsall,, N. S. Olesnicky,, A. Leibbrandt,, I. F. Connerton, and, L. A. Casselton. 1998. A large pheromone and receptor gene complex determines multiple B mating-type specificities in Coprinus cinereus. Genetics 148: 1081– 1090.

127. 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: 1242– 1248.

128. Perkins, D. D. 1984. Advantages of using the inactive-mating-type a m1 strain as a helper component in heterokaryons. Fungal Genet. Newsl. 31: 41– 42.

129. Perkins,, D. D. 1991. In praise of diversity, p. 3–26. In J. W. Bennett and, L. L. Lasure (ed.), More Gene Manipulations in Fungi. Academic Press, San Diego, CA.

130. Perkins, D. D. 1987. Mating-type switching in filamentous ascomycetes. Genetics 115: 215– 216.

131. Perkins,, D. D., and B. C. Turner. 1988. Neurospora from natural populations: toward the population biology of a haploid eukaryote. Exp. Mycol. 12: 91– 131.

132. Pieau, C., and, M. Dorizzi. 2004. Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J. Endocrinol. 181: 367– 377.

133. Pieau, C.,, M. Dorizzi, and, N. Richard-Mercier. 1999. Temperature-dependent sex determination and gonadal differentiation in reptiles. Cell. Mol. Life Sci. 55: 887– 900.

134. Pöggeler, S. 2001. Mating-type genes for classical strain improvements of ascomycetes. Appl. Microbiol. Biotechnol. 56: 589– 601.

135. Pöggeler,, S. 1999. Phylogenetic relationships between mating-type sequences from homothallic and heterothallic ascomycetes. Curr. Genet. 36: 222– 231.

136. Pöggeler, S. 2000. Two pheromone precursor genes are transcriptionally expressed in the homothallic ascomycete Sordaria macrospora. Curr. Genet. 37: 403– 411.

137. Pöggeler,, S., M. Nowrousian,, C. Ringelberg,, J. J. Loros,, J. C. Dunlap, and, U. Kück. 2006. Microarray and real-time PCR analyses reveal mating-type-dependent gene expression in a homothallic fungus. Mol. Genet. Genomics 275: 492– 503.

138. Pöggeler, S.,, S. Risch,, U. Kück, and H. D. Osiewacz. 1997. Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147: 567– 580.

139. Raju, N. B. 1992. Functional heterothallism resulting from homokaryotic conidia and ascospores in Neurospora tetrasperma. Mycol. Res. 96: 103– 116.

140. Raju,, N. B. 1992. Genetic control of the sexual cycle in Neurospora. Mycol. Res. 96: 241- 262.

141. Raju, N. B. 1980. Meiosis and ascospore genesis in Neurospora. Eur. J. Cell Biol. 23: 208– 223.

142. Raju,, N. B. 1978. Meiosis nuclear behaviour and ascospore formation in five homothallic species of Neurospora. Can. J. Bot. 56: 754– 763.

143. Raju, N. B., and, D. D. Perkins. 1994. Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Dev. Genet. 15: 104– 118.

144. Raper, C. A.,, J. R. Raper, and, R. E. Miller. 1972. Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 64: 1088- 1117.

145. Raper, J. R. 1966. Genetics of Sexuality in Higher Fungi. Ronald Press Co., New York, NY.

146. Raper, J. R., and, G. S. Krongelb. 1958. Genetic and environmental aspects of fruiting in Schizophyllum commune. Mycologia 50: 707– 740.

147. Raper, K. B., and, D. I. Fennell. 1965. The Genus Aspergillus. Williams & Wilkins, Baltimore, MD.

148. Robertson, S. J.,, D. J. Bond, and, N. D. Read. 1998. Homothallism and heterothallism in Sordaria brevicollis. Mycol. Res. 102: 1215– 1223.

149. Rusche, L. N.,, A. L. Kirchmaier, and, J. Rine. 2003. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu. Rev. Biochem. 72: 481– 516.

150. Rydholm, C.,, P. S. Dyer, and, F. Lutzoni. 2007. DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot. Cell 23 [Epub ahead of print].

151. Sarre, S. D.,, A. Georges, and, A. Quinn. 2004. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26: 639– 645.

152. Sharon, A.,, K. Yamaguchi,, S. Christiansen,, B. A. Horwitz,, O. C. Yoder, and, B. G. Turgeon. 1996. An asexual fungus has the potential for sexual development. Mol. Gen. Genet. 251: 60– 68.

153. 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: 366– 377.

154. Shimizu, K. K.,, J. M. Cork,, A. L. Caicedo,, C. A. Mays,, R. C. Moore,, K. M. Olsen,, S. Ruzsa,, G. Coop,, C. D. Bustamante,, P. Awadalla, and, M. D. Purugganan. 2004. Darwinian selection on a selfing locus. Science 306: 2081– 2084.

155. Shiu, P. K., and, N. L. Glass. 2000. Cell and nuclear recognition mechanisms mediated by mating type in filamentous ascomycetes. Curr. Opin. Microbiol. 3: 183– 188.

156. Smulian, A. G.,, T. Sesterhenn,, R. Tanaka, and, M. T. Cushion. 2001. The ste3 pheromone receptor gene of Pneumocystis carinii is surrounded by a cluster of signal transduction genes. Genetics 157: 991– 1002.

157. Staben, C., and, C. Yanofsky. 1990. Neurospora crassa a mating-type region. Proc. Natl. Acad. Sci. USA 87: 4917– 4921.

158. 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: 183– 197.

159. Strathern, J.,, J. Hicks, and, I. Herskowitz. 1981. Control of cell type in yeast by the mating type locus. The alpha 1-alpha 2 hypothesis. J. Mol. Biol. 147: 357– 372.

160. Strathern, J. N., and, I. Herskowitz. 1979. Asymmetry and directionality in production of new cell types during clonal growth: the switching pattern of homothallic yeast. Cell 17: 371– 381.

161. Strathern, J. N.,, A. J. Klar,, J. B. Hicks,, J. A. Abraham,, J. M. Ivy,, K. A. Nasmyth, and, C. McGill. 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31: 183– 192.

162. 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: 3219– 3224.

163. Szeto, L.,, M. K. Fafalios,, H. Zhong,, A. K. Vershon, and, J. R. Broach. 1997. Alpha2p controls donor preference during mating type interconversion in yeast by inactivating a recombinational enhancer of chromosome III. Genes Dev. 11: 1899– 1911.

164. Tellier, A.,, L. M. Villareal, and, T. Giraud. 2005. Maintenance of sex-linked deleterious alleles by selfing and group selection in metapopulations of the phytopathogenic fungus Microbotryum violaceum. Am. Nat. 165: 577– 589.

165. Thomas, C. F., Jr., and, A. H. Limper. 2004. Pneumocystis pneumonia. N. Engl. J. Med. 350: 2487– 2498.

166. Trail, F., and, R. Common. 2000. Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92: 130– 138.

167. 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: 230– 237.

168. Turgeon, B. G. 1998. Application of mating type gene technology to problems in fungal biology. Annu. Rev. Phytopathol. 36: 115– 137.

169. Turgeon,, B. G., H. Bohlmann,, L. M. Ciuffetti,, S. K. Christiansen,, G. Yang,, W. Schafer, and, O. C. Yoder. 1993. Cloning and analysis of the mating type genes from Cochliobolus heterostrophus. Mol. Gen. Genet. 238: 270– 284.

170. Ullrich, R. C. 1973. Sexuality, incompatibility, and intersterility in the biology of the Sistotrema brinkmannii aggregate. Mycologia 65: 1234– 1249.

171. Ullrich, R. C., and, J. R. Raper. 1975. Primary homothallism—relation to heterothallism in the regulation of sexual morphogenesis in Sistotremai. Genetics 80: 311– 321.

172. Uno, I., and, T. Ishikawa. 1971. Chemical and genetical control of induction of monokaryotic fruiting bodies in Coprinus macrorhizus. Mol. Gen. Genet. 113: 229– 239.

173. Uno, I., and, T. Ishikawa. 1973. Metabolism of adeno-sine 3′,5′-cyclic monophosphate and induction of fruiting bodies in Coprinus macrorhizus. J. Bacteriol. 113: 1249– 1255.

174. Uno, I., and, T. Ishikawa. 1973. Purification and identification of the fruiting-inducing substances in Coprinus macrorhizus. J. Bacteriol. 113: 1240– 1248.

175. 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: 73– 78.

176. Varga,, J., and B. Toth. 2003. Genetic variability and reproductive mode of Aspergillus fumigatus. Infect. Genet. Evol. 3: 3– 17.

177. Vengrova, S., and, J. Z. Dalgaard. 2004. RNase-sensitive DNA modification(s) initiates S. pombe mating-type switching. Genes Dev. 18: 794– 804.

178. Vengrova, S., and, J. Z. Dalgaard. 2006. The wild-type Schizosaccharomyces pombe mat1 imprint consists of two ribonucleotides. EMBO Rep. 7: 59– 65.

179. 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: 331– 335.

180. 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: 352– 362.

181. Wessels, J. G. 1993. Fruiting in the higher fungi. Adv. Microb. Physiol. 34: 147– 202.

182. Wickes,, B. L., U. Edman, and, J. C. Edman. 1997. The Cryptococcus neoformans STE12alpha gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol. Microbiol. 26: 951– 960.

183. 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: 7327– 7331.

184. Wu, C.,, K. Weiss,, C. Yang,, M. A. Harris,, B. K. Tye,, C. S. Newlon,, R. T. Simpson, and, J. E. Haber. 1998. Mcm1 regulates donor preference controlled by the recombination enhancer in Saccharomyces mating-type switching. Genes Dev. 12: 1726– 1737.

185. Wyder, M. A.,, E. M. Rasch, and, E. S. Kaneshiro. 1998. Quantitation of absolute Pneumocystis carinii nuclear DNA content. Trophic and cystic forms isolated from infected rat lungs are haploid organisms. J. Eukaryot. Microbiol. 45: 233– 239.

186. Xu, J.,, R. W. Kerrigan,, P. A. Horgen, and, J. B. Anderson. 1993. Localization of the mating type gene in Agaricus bisporus. Appl. Environ. Microbiol. 59: 3044– 3049.

187. Yun, S. H.,, T. Arie,, I. Kaneko,, O. C. Yoder, and, B. G. Turgeon. 2000. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/ Fusarium species. Fungal Genet. Biol. 31: 7– 20.

188. Yun, S. H.,, M. L. Berbee,, O. C. Yoder, and, B. G. Turgeon. 1999. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc. Natl. Acad. Sci. USA 96: 5592– 5597.

189. Zickler, D.,, S. Arnaise,, E. Coppin,, R. Debuchy, and, M. Picard. 1995. Altered mating-type identity in the fungus Podospora anserina leads to selfish nuclei, uniparental progeny, and haploid meiosis. Genetics 140: 493– 503.