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Chapter 2 : Evolution of the Mating-Type Locus: The Basidiomycetes

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Evolution of the Mating-Type Locus: The Basidiomycetes, Page 1 of 2

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Abstract:

Of all the fungi, production of sexual structures is most prominent in the members of the phylum . The sexual cycles of fungi have been well studied for several decades. Research has shown that although enormous variation exists between the sexual processes of different fungal species, there are two common, underlying paradigms: the bipolar and the tetrapolar mating-type systems. The sexual cycles of fungi have been well studied for several decades. Research has shown that although enormous variation exists between the sexual processes of different fungal species, there are two common, underlying paradigms: the bipolar and the tetrapolar mating-type systems. In a typical basidiomycete sexual cycle, cells undergo chemoattraction, fuse to form a dikaryon, and nuclear migration is orchestrated by a complex regulatory process involving clamp cell formation and fusion. The genes encoding pheromone produce an immature product that requires extensive posttranslational modification, with the immature peptide undergoing prenylation, proteolytic cleavage, and carboxy-terminal methylation to produce the mature, biologically active form. is a phytopathogen that infects maize plants, a process that occurs only when the fungus is in the dikaryotic filamentous phase produced by mating. The smut is closely related to and infects both maize and sorghum. Unlike its better-known relative, the role of the sexual cycle in infection in is currently unknown, but the potential link between infection and mating has encouraged analysis of the mating-type system in this pathogen.

Citation: Fraser J, Hsueh Y, Findley K, Heitman J. 2007. Evolution of the Mating-Type Locus: The Basidiomycetes, p 19-34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch2
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Figures

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Figure 2.1

Life cycle of basidiomycetous fungi. Haploid cells of opposite mating type fuse, often via the action of the pheromone/receptor locus, to produce a filamentous dikaryon. The process of clamp cell formation and fusion (also under the control of the pheromone/receptor gene locus) functions to ensure the integrity of nuclear transmission in the dikaryon. The homeodomain locus is required for clamp cell formation and septation and to maintain the dikaryon once it has formed following nuclear division. The structure in which meiosis occurs, the basidium, is then formed, and the two nuclei fuse. Meiosis ensues, generating four nuclei, which ultimately give rise to basidiospores. These spores later germinate to produce individual haploid cells.

Citation: Fraser J, Hsueh Y, Findley K, Heitman J. 2007. Evolution of the Mating-Type Locus: The Basidiomycetes, p 19-34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch2
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Image of Figure 2.2
Figure 2.2

Schematic representation of loci in the model tetrapolar basidiomycetes. The top panel depicts the homeodomain protein loci; arrows represent divergently transcribed homeodomain protein pairs. The bottom panel depicts the pheromone and pheromone receptor loci; the longer dotted arrows represent pheromone receptors, and the shorter solid arrows represent pheromone genes. Note that in both loci, segmental duplication events are evident in the evolution of .

Citation: Fraser J, Hsueh Y, Findley K, Heitman J. 2007. Evolution of the Mating-Type Locus: The Basidiomycetes, p 19-34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch2
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Image of Figure 2.3
Figure 2.3

Model for the evolution of in . has evolved via four main steps, beginning with gene acquisition into two unlinked sex-determining regions, forming two discrete gene clusters involved in mating. Next, these fused into a single structure via a chromosomal translocation in one mating type. The translocation resulted in a tripolar intermediate state that was converted to a bipolar system via gene conversion between the linked and unlinked sex-determining regions. Lastly, has been subjected to ongoing intra- and interallelic gene conversion and inversions that suppress recombination.

Citation: Fraser J, Hsueh Y, Findley K, Heitman J. 2007. Evolution of the Mating-Type Locus: The Basidiomycetes, p 19-34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch2
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Figure 2.4

recombination may trigger transitions between bipolar and tetrapolar, and homothallic-heterothallic mating systems. Recombination at either of the loci in a tetrapolar basidiomycete may lead to self-activation of one of the loci, which transforms the mating system to bipolar. Similarly, recombination events at both loci would convert a tetrapolar heterothallic basidiomycete to a homothallic life cycle.

Citation: Fraser J, Hsueh Y, Findley K, Heitman J. 2007. Evolution of the Mating-Type Locus: The Basidiomycetes, p 19-34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch2
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References

/content/book/10.1128/9781555815837.ch02
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. 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.
3. Asada, Y.,, C. Yue,, J. Wu,, G. P. Shen,, C. P. Novotny, and, R. C. Ullrich. 1997. Schizophyllum commune A alpha mating-type proteins, Y and Z, form complexes in all combinations in vitro. Genetics 147:117123.
4. Bakkeren, G.,, G. Jiang,, R. L. Warren,, Y. Butterfield,, H. Shin,, R. Chiu,, R. Linning,, J. Schein,, N. Lee,, G. Hu,, D. M. Kupfer,, Y. Tang,, B. A. Roe,, S. Jones,, M. Marra, and, J. W. Kronstad. 2006. Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet. Biol. 43:655666.
5. Bakkeren, G., and, J. W. Kronstad. 1993. Conservation of the b mating-type gene complex among bipolar and tetrapolar smut fungi. Plant Cell 5:123136.
6. Bakkeren, G., and, J. W. Kronstad. 1994. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc. Natl. Acad. Sci. USA 91:70857089.
7. Banuett, F. 1992. Ustilago maydis, the delightful blight. Trends Genet. 8:174180.
8. Bolker, M.,, M. Urban, and, R. Kahmann. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441450.
9. Bortfeld, M.,, K. Auffarth,, R. Kahmann, and, C. W. Basse. 2004. The Ustilago maydis a2 mating-type locus genes lga2 and rga2 compromise pathogenicity in the absence of the mitochondrial p32 family protein Mrb1. Plant Cell 16:22332248.
10. Brown, A. J., and, L. A. Casselton. 2001. Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet. 17:393400.
11. Brown, D. W.,, J. H. Yu,, H. S. Kelkar,, M. Fernandes,, T. C. Nesbitt,, N. P. Keller,, T. H. Adams, and, T. J. Leonard. 1996. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 93:14181422.
12. Burnett, J. H. 1975. Mycogenetics. John Wiley & Sons, London, United Kingdom.
13. 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 101:16321637.
14. Casselton, L. A., and, N. S. Olesnicky. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62:5570.
15. Dooijes, D.,, M. van de Wetering,, L. Knippels, and, H. Clevers. 1993. The Schizosaccharomyces pombe mating-type gene mat-Mc encodes a sequence-specific DNA-binding high mobility group box protein. J. Biol. Chem. 268:2481324817.
16. Feldbrugge, M.,, J. Kamper,, G. Steinberg, and, R. Kahmann. 2004. Regulation of mating and pathogenic development in Ustilago maydis. Curr. Opin. Microbiol. 7:666672.
17. 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 10:25592572.
18. Fowler, T. J.,, M. F. Mitton,, L. J. Vaillancourt, and, C. A. Raper. 2001. Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics 158:14911503.
19. 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. 2:22432255.
20. Fraser, J. A., and, J. Heitman. 2003. Fungal mating-type loci. Curr. Biol. 13:R792R795.
21. Gardiner, D. M.,, A. J. Cozijnsen,, L. M. Wilson,, M. S. Pedras, and, B. J. Howlett. 2004. The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol. Microbiol. 53:13071318.
22. Gillissen, B.,, J. Bergemann,, C. Sandmann,, B. Schroeer,, M. Bolker, and, R. Kahmann. 1992. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68:647657.
23. Gola, S.,, J. Hegner, and, E. Kothe. 2000. Chimeric pheromone receptors in the basidiomycete Schizophyllum commune. Fungal Genet. Biol. 30:191196.
24. Herskowitz, I.,, J. Rine, and, J. N. Strathern. 1992. Mating Type Determination and Mating-Type Interconversion in Saccharomyces cerevisiae, vol. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Hood, M. E. 2002. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160:457461.
26. Hood,, M. E. 2005. Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:110.
27. 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 168:141146.
28. Horn, F.,, E. Bettler,, L. Oliveira,, F. Campagne,, F. E. Cohen, and, G. Vriend. 2003. GPCRDB information system for G protein-coupled receptors. Nucleic Acids Res. 31:294297.
29. Hsueh, Y. P.,, A. Idnurm, and, J. Heitman. 2006. Recombination hot spots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLoS Genet. 2:e184.
30. Hsueh, Y. P., and, W. C. Shen. 2005. 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 4:147155.
31. Hull, C. M., and, A. D. Johnson. 1999. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285:12711275.
32. 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.
33. Iwase, M.,, Y. Satta,, Y. Hirai,, H. Hirai,, H. Imai, and, N. Takahata. 2003. The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species. Proc. Natl. Acad. Sci. USA 100:52585263.
34. 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.
35. Kamada, T. 2002. Molecular genetics of sexual development in the mushroom Coprinus cinereus. Bioessays 24:449459.
36. Kamper,, J., R. Kahmann,, M. Bolker,, L. J. Ma,, T. Brefort,, B. J. Saville,, F. Banuett,, J. W. Kronstad,, S. E. Gold,, O. Muller,, M. H. Perlin,, H. A. Wosten,, R., de Vries,, J. Ruiz-Herrera,, C. G. Reynaga-Pena,, K. Snetselaar,, M. McCann,, J. Perez-Martin,, M. Feldbrugge,, C. W. Basse,, G. Steinberg,, J. I. Ibeas,, W. Holloman,, P. Guzman,, M. Farman,, J. E. Stajich,, R. Sentandreu,, J. M. Gonzalez-Prieto,, J. C. Kennell,, L. Molina,, J. Schirawski,, A. Mendoza-Mendoza,, D. Greilinger,, K. Munch,, N. Rossel,, M. Scherer,, M. Vranes,, O. Ladendorf,, V. Vincon,, U. Fuchs,, B. Sandrock,, S. Meng,, E. C. Ho,, M. J. Cahill,, K. J. Boyce,, J. Klose,, S. J. Klosterman,, H. J. Deelstra,, L. Ortiz-Castellanos,, W. Li,, P. Sanchez-Alonso,, P. H. Schreier,, I. Hauser-Hahn,, M. Vaupel,, E. Koopmann,, G. Friedrich,, H. Voss,, T. Schluter,, J. Margolis,, D. Platt,, C. Swimmer,, A. Gnirke,, F. Chen,, V. Vysotskaia,, G. Mannhaupt,, U. Guldener,, M. Munsterkotter,, D. Haase,, M. Oesterheld,, H. W. Mewes,, E. W. Mauceli,, D. DeCaprio,, C. M. Wade,, J. Butler,, S. Young,, D. B. Jaffe,, S. Calvo,, C. Nusbaum,, J. Galagan, and, B. W. Birren. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97101.
37. Kamper, J.,, M. Reichmann,, T. Romeis,, M. Bolker, and, R. Kahmann. 1995. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:7383.
38. Kothe, E. 1999. Mating types and pheromone recognition in the homobasidiomycete Schizophyllum commune. Fungal Genet. Biol. 27:146152.
39. Kothe,, E. 1996. Tetrapolar fungal mating types: sexes by the thousands. FEMS Microbiol. Rev. 18:6587.
40. Kues, U.,, B. Gottgens,, R. Stratmann,, W. V. Richardson,, S. F. O’Shea, and L. A. Casselton. 1994. A chimeric homeodomain protein causes self-compatibility and constitutive sexual development in the mushroom Coprinus cinereus. EMBO J. 13:40544059.
41. Lee, N.,, G. Bakkeren,, K. Wong,, J. E. Sherwood, and, J. W. Kronstad. 1999. The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc. Natl. Acad. Sci. USA 96:1502615031.
42. 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.
43. 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 1:704718.
44. Loftus, B. J.,, E. Fung,, P. Roncaglia,, D. Rowley,, P. Amedeo,, D. Bruno,, J. Vamathevan,, M. Miranda,, I. J. Anderson,, J. A. Fraser,, J. E. Allen,, I. E. Bosdet,, M. R. Brent,, R. Chiu,, T. L. Doering,, M. J. Donlin,, C. A., D’Souza,, D. S. Fox,, V. Grinberg,, J. Fu,, M. Fukushima,, B. J. Haas,, J. C. Huang,, G. Janbon,, S. J. Jones,, H. L. Koo,, M. I. Krzywinski,, J. K. Kwon-Chung,, K. B. Lengeler,, R. Maiti,, M. A. Marra,, R. E. Marra,, C. A. Mathewson,, T. G. Mitchell,, M. Pertea,, F. R. Riggs,, S. L. Salzberg,, J. E. Schein,, A. Shvartsbeyn,, H. Shin,, M. Shumway,, C. A. Specht,, B. B. Suh,, A. Tenney,, T. R. Utterback,, B. L. Wickes,, J. R. Wortman,, N. H. Wye,, J. W. Kronstad,, J. K. Lodge,, J. Heitman,, R. W. Davis,, C. M. Fraser, and, R. W. Hyman. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:13211324.
45. 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.
46. Martinez, D.,, L. F. Larrondo,, N. Putnam,, M. D. Gelpke,, K. Huang,, J. Chapman,, K. G. Helfenbein,, P. Ramaiya,, J. C. Detter,, F. Larimer,, P. M. Coutinho,, B. Henrissat,, R. Berka,, D. Cullen, and, D. Rokhsar. 2004. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat. Biotechnol. 22:695700.
47. Murphy, J., and, O. J. Miller. 1997. Diversity and local distribution of mating alleles in Marasmiellus praeacutus and Collybia subnuda (Basidiomycetes, Agaricales). Can. J. Bot. 75:817.
48. Ohno, S. 1970. Evolution by Gene Duplication. Allen and Unwin, London, United Kingdom.
49. Ohno, S. 1967. Sex Chromosomes and Sex-Linked Genes. Springer-Verlag, New York, NY.
50. Olesnicky, N. S.,, A. J. Brown,, Y. Honda,, S. L. Dyos,, S. J. Dowell, and, L. A. Casselton. 2000. Self-compatible B mutants in coprinus with altered pheromone-receptor specificities. Genetics 156:10251033.
51. Raper, J. 1966. Genetics of Sexuality in Higher Fungi. The Ronald Press, New York, NY.
52. Robertson, C. I.,, K. A. Bartholomew,, C. P. Novotny, and, R. C. Ullrich. 1996. Deletion of the Schizophyllum commune Aα locus: the roles of Aα Y and Z mating-type genes. Genetics 144:14371444.
53. Rozen, S.,, H. Skaletsky,, J. D. Marszalek,, P. J. Minx,, H. S. Cordum,, R. H. Waterston,, R. K. Wilson, and, D. C. Page. 2003. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423:873876.
54. Schirawski, J.,, B. Heinze,, M. Wagenknecht, and, R. Kahmann. 2005. Mating type loci of Sporisorium reilianum: novel pattern with three a and multiple b specificities. Eukaryot. Cell 4:13171327.
55. Shen, G. P.,, D. C. Park,, R. C. Ullrich, and, C. P. Novotny. 1996. Cloning and characterization of a Schizophyllum gene with A beta 6 mating-type activity. Curr. Genet. 29:136142.
56. Staben, C., and, C. Yanofsky. 1990. Neurospora crassa a mating-type region. Proc. Natl. Acad. Sci. USA 87:49174921.
57. Ullrich, R., and, J. Raper. 1974. Number and distribution of bipolar incompatibility factors in Sistotrema brinkmannii. Am. Nat. 108:507518.
58. Urban, M.,, R. Kahmann, and, M. Bolker. 1996. The biallelic a mating type locus of Ustilago maydis: remnants of an additional pheromone gene indicate evolution from a multiallelic ancestor. Mol. Gen. Genet. 250:414420.
59. Wong, S., and, K. H. Wolfe. 2005. Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat. Genet. 37:777782.

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