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Chapter 17 : The Origin of Multiple Mating Types in the Model Mushrooms and

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Abstract:

Historically, ( sensu , ) and were the first hymenomycete species shown to be heterothallic, and it is not surprising that studies on mating type have, until recently, focused on these two species. It was Hans Kniep who recognized that the matingtype genes were multiallelic and many different mating types existed in the population. Kniep’s remarkably thorough studies, involving analyzing progeny from many generations of crosses, led him to note that some 1 to 2% of the progeny of sexual crosses in had new mating types, and he naturally attributed this to mutation. Haploid basidiospores germinate to give a self-sterile mycelium that is generally called a monokaryon because it has predominantly uninucleate cells. Mushrooms appear to be unique among fungi in having evolved multiple versions of their pheromones and receptors, and this has been driven by the need to increase the numbers of mating types. The genome sequence of reveals several clusters of genes of related function, suggesting that gene amplification has contributed to many aspects of the biology of this fungus. The majority of hymenomycetes are heterothallic, and it seems likely that as in ascomycetes, homothallic species were derived from heterothallic species. With the molecular and genomic tools we now have, exploring deeper into the study of the loci enhances one's understanding of the importance of sex and its involvement in genome evolution.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Figures

Image of Figure 17.1
Figure 17.1

Life cycle of . Photographs were taken by J. D. Granado, E. Polak, P. Srivilai, and W. Chaisaena.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Image of Figure 17.2
Figure 17.2

Archetypal organization of the and mating-type loci of . (A) locus composed of three subloci each containing two divergently transcribed genes encoding dissimilar homeodomain proteins. The genes are distinguished as and based on the conserved but different protein homeodomains, and the three paralogous pairs of genes are designated the , , and pairs. Horizontal arrows indicate the direction of transcription, and fill motifs are used to differentiate allelic and paralogous versions of the genes. Crossed arrows indicate the compatible gene pairs that encode subunits of an active transcription factor complex formed after cell fusion. (B) locus composed of three subloci each containing a receptor gene and two pheromone genes. The three paralogous receptor genes are designated , , and . The corresponding pheromone genes are designated , , and with different genes given the additional numbers (i.e., and ) to represent order with respect to . Horizontal arrows indicate the direction of transcription; fill motifs are used to indicate different allelic and paralogous versions of the genes. Crossed arrows indicate receptor and pheromone combinations that can activate development upon mating.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Figure 17.3

Comparison of sequenced mating-type loci of . (A) and . , , , and are genes. , , and are genes. Fill motifs denote allelic and paralogous versions of the genes. and have replicate alleles of the gene, , in sublocus 3 but have different alleles of genes in sublocus 1 and 2. There are three compatible gene combinations indicated by diagonal arrows. (B) and . , , , and are receptor genes, and pheromone genes are designated followed by the sublocus and position numbers. , shown in parentheses, is predicted to be a pseudogene. Alleles of genes at all three subloci are different, as indicated by different fill motifs, and all generate compatible receptor-pheromone combinations (shown by vertical arrows). Horizontal arrows indicate the direction of gene transcription. and are non-mating-type genes that flank the locus.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Figure 17.4

Pheromone precursor sequences from (A) and (B). The amino acid sequences are highly variable in length and sequence. The sequence of the mature pheromone is given in larger type; the predicted N-terminal recognition site, a charged doublet that is generally ER in , and the subterminal doublet are presented in bold. The CaaX motif is underlined.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Image of Figure 17.5
Figure 17.5

PAUP*maximum parsimony analysis of receptor proteins. A strict consensus tree is shown with bootstrap support values (percentage of 1,000 replicates) in italics. The nominated outgroup was Ste3p. Rcb alleles are distinguished by superscripts that denote the wild-type specificity from which the genes were sequenced. Analysis by M. P. Challen.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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Figure 17.6

The self-fertile homokaryon AmutBmut of (, , and ) ( ) forms fruiting bodies under suitable environmental conditions (day-night rhythm, 25 to 28°C, >80% humidity). Localized hyphal branching gives rise to loose aggregates (primary hyphal knots). A light signal is needed (day 0) for appearance of compact secondary hyphal knots (day 1 of development). Over the next 5 days, cap and stipe tissues differentiate. Tissue differentiation is light controlled: when light is lacking, structures known as etiolated stipes or dark stipes are formed with elongated stipe bases terminating in rudimentary stipes and caps. The light signal at day 5 gives rise to karyogamy, meiosis, and basidospore formation at day 6 of development. During meiosis and basidiospore formation, the mushroom cap expands and the stipe elongates to give shortly after midnight a fully matured fruiting body. Fruiting bodies are short-lived and undergo autolysis on day 7 of development in order to disperse the black basidiospores. UV and REMI mutagenesis of oidia from this strain has yielded over 9,000 different clones that have been individually tested for fruiting behavior. Several hundreds of mutants were obtained and grouped into categories according to the developmental stage affected (U. Kües, J. D. Granado, and M. Aebi, unpublished data). Mutants in the Amut Bmut background mentioned in the text are characterized by lack of secondary hyphal knot formation (), formation of etiolated stipes in the light (), formation of mushrooms with a short stipe that is unable to elongate (), and white caps that lack basidiospores (). The time course of fruiting-body development of homokaryon AmutBmut was kindly supplied by M. Navarro-González, and the photograph of the etiolated stipe was kindly supplied by W. Chaisaena.

Citation: Casselton L, Kües U. 2007. The Origin of Multiple Mating Types in the Model Mushrooms and , p 283-300. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch17
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References

/content/book/10.1128/9781555815837.ch17
1. Arima, T.,, M. Yamamoto,, A. Hirata,, S. Kawano, and, T. Kamada. 2004. The eln3 gene involved in fruiting body morphogenesis of Coprinus cinereus encodes a putative membrane protein with a general glycosyltransferase domain. Fungal Genet. Biol. 41:805812.
2. Asante-Owusu, R. N. 1994. Manipulation of the A mating type genes of Coprinus cinereus. Ph.D. thesis. University of Oxford, Oxford, United Kingdom.
3. Asante-Owusu, R. N.,, A. H. Banham,, H. U. Böhnert, E. J. C. Mellor, and, L. A. Casselton. 1996. Heterodimerization between two classes of homeodomain proteins in the mushroom Coprinus cinereus brings together potential DNA-binding and activation domains. Gene 172:2531.
4. Badalyan, S. M.,, E. Polak,, R. Hermann,, M. Aebi, and, U. Kües. 2004. Role of peg formation in clamp cell fusion of homeobasidiomycete fungi. J. Basic Microbiol. 44:167177.
5. Badrane, H., and, G. May. 1999. The divergence-homogenization duality in the evolution of the b1 mating type of Coprinus cinereus. Mol. Biol. Evol. 16:975986.
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. 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. doi:10.1016/j.fgb.2006.04.002.
8. Banham, A. H.,, R. N. Asante-Owusu,, B. Göttgens, S. A. J. Thompson,, C. S. Kingsnorth,, E. J. C. Mellor, and, L. A. Casselton. 1995. An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell 7:773783.
9. Bardwell, L. 2004. A walk-through of the yeast mating pheromone response pathway. Peptides 25:14651476.
10. Bensaude,, M. 1918. Recherches sur le cycle évolutif et la sexualité chez les Basidiomycètes. Ph.D. thesis. Faculté des Sciences de Paris, Imprimerie Nemourienne, Henri Bouloy, Nemours, France.
11. Bölker, M.,, M. Urban, and, R. Kahmann. 1992. The a mating type locus of U. maydis specifies cell signalling components. Cell 68:441450.
12. Brachmann, A.,, G. Weinzierl,, J. Kämper, and R. Kahmann. 2001. Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42:10471063.
13. Brown, A. J., and, L. A. Casselton. 2001. Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet. 17:393400.
14. Buller, H. R. 1931. Researches on Fungi. IV. Further Observations on the Coprini Together with Some Investigations on Social Organisation and Sex in the Hymenomycetes. Hafner Publishing Co., New York, NY.
15. Caldwell, G. A.,, F. Naider, and, J. M. Becker. 1995. Fungal lipopetide mating pheromones: a model system for the study of protein prenylation. Microbiol. Rev. 59:406422.
16. Casselton, L. A., and, N. S. Olesnicky. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62:5570.
17. Casselton, L. A., and, M. Zolan. 2002. The art and design of genetic screens: filamentous fungi. Nat. Rev. Genet. 3:683697.
18. Celerin, M.,, S. T. Merino,, J. F. Stone,, A. M. Menzie, and, M. F. Zolan. 2000. Multiple roles of Spo11 in meiotic chromosome behavior. EMBO J. 19:27392750.
19. Chen, P.,, S. K. Sapperstein,, J. D. Choi, and, S. Michaelis. 1997. Biogenesis of the Saccharomyces cerevisiae mating pheromone a-factor. J. Cell Biol. 136:251269.
20. Cummings, W. J.,, M. Celerin,, J. Crodian,, L. K. Brunick, and, M. E. Zolan. 1999. Insertional mutagenesis in Coprinus cinereus: use of a dominant selection marker to generate tagged sporulation defective mutants. Curr. Genet. 36:371382.
21. Day, P. 1961. The structure of the A mating-type locus of Coprinus lagopus. Genetics 45:641650.
22. Day,, P. R. 1963. Mutations affecting the A mating-type locus in Coprinus lagopus. Genet. Res. 4:5565.
23. Day, P. R. 1963. The structure of the A mating type factor in Coprinus lagopus: wild alleles. Genet. Res. 4:323325.
24. 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.), The Mycota. 1. Growth, Differentiation and Sexuality, 2nd ed. Springer-Verlag, Berlin, Germany.
25. Dowell, S. J., and, A. J. Brown. 2002. Yeast assays for G-protein-coupled receptors. Recept. Channels 8:343352.
26. Duboule, D. 1994. Guidebook to the Homeobox Genes. Oxford University Press, Oxford, England.
27. Feldbrügge, M.,, M. Bölker, G. Steinberg,, J. Kämper, and R. Kahmann. 2006. Regulatory and structural networks orchestrating mating, dimorphism, cell shape and pathogenesis in Ustilago maydis, p. 375–391. In U. Kües and R. Fischer (ed.), The Mycota. 1. Growth, Differentiation and Sexuality, 2nd ed. Springer-Verlag, Berlin, Germany.
28. 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.
29. Fowler, T. J.,, M. J. 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.
30. Fowler, T. J.,, M. F. Mitton,, E. I. Rees, and, C. A. Raper. 2004. Crossing the boundary between the and mating-type loci in Schizophyllum commune. Fungal Genet. Biol. 41:89101.
31. Freedman, T., and, P. J. Pukkila. 1997. A physical assay for meiotic recombination in Coprinus cinereus. Mol. Gen. Genet. 254:372378.
32. Garcia-Muse, T.,, G. Steinberg, and, J. Perez-Martin. 2003. Pheromone-induced G(2) arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot. Cell 2:494500.
33. Giasson, L.,, C. A. Specht,, C. Milgrim,, C. P. Novotny, and, R. C. Ullrich. 1989. Cloning and comparison of Aα mating-type alleles of the basidiomycete Schizophyllum commune. Mol. Gen. Genet. 218:7277.
34. Giesy, R. M., and, P. R. Day. 1965. The septal pores of Coprinus lagopus (Fr.) sensu Buller in relation to nuclear migration. Am. J. Bot. 52:287293.
35. Gillissen, B.,, J. Bergemann,, C. Sandmann,, B. Schroeer,, M. Bölker, and R. Kahmann. 1992. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68:647657.
36. Granado, J. D.,, K. Kertesz-Chaloupková, M. Aebi, and, U. Kües. 1997. Restriction enzyme-mediated DNA integration in Coprinus cinereus. Mol. Gen. Genet. 256:2836.
37. Halsall, J. R.,, M. J. Milner, and, L. A. Casselton. 2000. Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics 154:11151123.
38. Haylock, R. W.,, A. Economou, and, L. A. Casselton. 1980. Dikaryon formation in Coprinus cinereus: selection and identification of B factor mutants. J. Gen. Microbiol. 121:1726.
39. Herskowitz, I. 1988. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52:536553.
40. Hoffman,, R. M., and J. R. Raper. 1974. Genetic impairment of energy conservation in development of Schizophyllum. Efficient mitochondria in energy-starved cells. J. Gen. Microbiol. 82:6775.
41. Hull, C. M.,, M. J. Boily, and, J. Heitman. 2005. Sexspecific homeodomain proteins Sxi1α and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot. Cell 4:526535.
42. 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.
43. Iwasa, M.,, S. Tanabe, and, T. Kamada. 1998. The two nuclei in the dikaryon of the homobasidiomycete Coprinus cinereus change position after each conjugate division. Fungal Genet. Biol. 23:110116.
44. James, T. Y.,, S. R. Liou, and, R. Vilgalys. 2004. The genetic structure and diversity of the A and B mating-type genes from the tropical oyster mushroom, Pleurotus djamor. Fungal Genet. Biol. 41:813825.
45. James, T. Y.,, P. Srivilai,, U. Kües, 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.
46. Johnson, A. D. 1995. Molecular mechanisms of cell-type determination in budding yeast. Curr. Opin. Genet. Dev. 5:552558.
47. Kaffarnik,, F., P. Müller, M. Leibundgut,, R. Kahmann, and, M. Feldbrügge. 2003. PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J. 22:58175826.
48. Kämper, J.,, M. Reichmann,, T. Romeis,, M. Bölker, and R. Kahmann. 1995. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:7383.
49. Kanda, T.,, A. Goto,, K. Sawa,, H. Arakawa,, Y. Yasuda, and, T. Takemaru. 1989. Isolation and characterization of recessive sporeless mutants in the basidiomycete Coprinus cinereus. Mol. Gen. Genet. 216:526529.
50. Kanda, T.,, H. Arakawa,, Y. Yasuda, and, T. Takemaru. 1990. Basidiospore formation in a mutant of incompatibility factors and in mutants that arrest at metaphase I in Coprinus cinereus. Exp. Mycol. 14:218226.
51. Ke, A., and, C. Wolberger. 2003. Insights into binding cooperativity of MATa1/MATα2 from the crystal structure of a MATa1 homeodomain-maltose binding protein chimera. Protein Sci. 12:306312.
52. Kertesz-Chaloupková, K.,, P. J. Walser,, J. D. Granado,, M. Aebi, and, U. Kües. 1998. Blue light overrides repression of asexual sporulation by mating type genes in the basidiomycete Coprinus cinereus. Fungal Genet. Biol. 23:95109.
53. Kilaru, S.,, P. J. Hoegger, and, U. Kües. 2006. The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr. Genet. 50:4560.
54. Kimura, K. 1952. Studies on the sex of Coprinus macrorhizus Rea f. microsporus Hongo. I. Introductory experiments. Biol. J. Okayama Univ. 1:7279.
55. Kniep,, H. 1928. Die Sexualität der niederen Pflanzen. Fischer, Jena, Germany.
56. Koltin, Y. 1968. The genetic structure of the incompatibility factors of Schizophyllum commune. Comparative studies of primary mutations in the B factor. Mol. Gen. Genet. 102:196203.
57. Koltin,, Y., and J. R. Raper. 1967. The genetic structure of incompatibility factors of Schizophyllum commune: three functionally distinct classes of B factors. Proc. Natl. Acad. Sci. USA 58:12201226.
58. Koltin, Y.,, J. Stamberg,, N. Bawnick,, R. Tamarkin, and, R. Werczberger. 1979. Mutational analysis of natural alleles in and affecting the B incompatibility factor of Schizophyllum. Genetics 93:383391.
59. Kothe, E.,, S. Gola, and, J. Wendland. 2003. Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi. Curr. Genet. 42:268275.
60. Kües, U. 2000. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64:316353.
61. Kües,, U., and L. A. Casselton. 1992. Homeodomains and regulation of sexual development in basidiomycetes. Trends Genet. 8:154155.
62. Kües, U., and, L. A. Casselton. 1993. The origin of multiple mating types in mushrooms. J. Cell Sci. 104:227230.
63. Kües, U.,, W. V. J. Richardson,, A. M. Tymon,, E. S. Mutasa,, B. Göttgens, S. Gaubatz,, A. Gregoriades, and, L. A. Casselton. 1992. The combination of dissimilar alleles of the and gene complexes, whose proteins contain homeodomain motifs, determines sexual development in the mushroom Coprinus cinereus. Genes Dev. 4:568577.
64. Kües, U.,, R. N. Asante-Owusu,, E. S. Mutasa,, A. M. Tymon,, E. H. Pardo,, S. F. O’Shea, and L. A. Casselton. 1994. Two classes of homeodomain proteins specify the multiple A mating types of the mushroom Coprinus cinereus. Plant Cell 6:14671475.
65. Kües, U.,, B. Göttgens, R. Stratmann,, W. V. J. 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.
66. Kües, U.,, A. M. Tymon,, W. V. J. Richardson,, G. May,, P. T. Geiser, and, L. A. Casselton. 1994. A mating-type factors of Coprinus cinereus have variable numbers of specificity genes encoding two classes of homeodomain proteins. Mol. Gen. Genet. 245:4552.
67. Kües, U.,, P. J. Walser,, M. J. Klaus, and, M. Aebi. 2002. Influence of activated A and B mating type pathways on developmental processes in the basidiomycete Coprinus cinereus. Mol. Genet. Genomics 268:262271.
68. Kües, U.,, M. Navarro-González, P. Srivilai,, W. Chaisaena, and, R. Velagapudi. 2006. Mushroom biology and genetics. In U. Kües (ed.), Wood Production, Wood Technology and Biotechnological Impacts. Universitätsverlag Göttingen, Göttingen, Germany.
69. Kurjan, J. 1993. The pheromone response pathway in Saccharomyces cerevisiae. Annu. Rev. Genet. 27:147179.
70. 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.
71. Liu, Y.,, P. Srivilai,, S. Loos,, M. Aebi, and, U. Kües. 2006. An essential gene for fruiting initiation in the basidiomycete Coprinopsis cinerea is homologous to bacterial cyclopropane fatty acid synthase genes. Genetics 172:873884.
72. Lu, B. C.,, N. Gallo, and, U. Kües. 2003. White-cap mutants and meiotic apoptosis in the fungus Coprinus cinereus. Fungal Genet. Biol. 39:8293.
73. Luo, Y. H.,, R. C. Ullrich, and, C. P. Novotny. 1994. Only one of the paired Schizophyllum commune Aα mating-type putative homeobox genes encodes a homeodomain essential for regulated development. Mol. Gen. Genet. 244:318324.
74. Magae, Y.,, C. Novotny, and, R. Ullrich. 1995. Interaction of the A alpha Y mating-type and Z mating-type homeodomain proteins of Schizophyllum commune detected by the two-hybrid system. Biochem. Biophys. Res. Commun. 211:10711076.
75. May, G., and, E. Matzke. 1995. Recombination and variation at the A mating-type locus of Coprinus cinereus. Mol. Biol. Evol. 12:794802.
76. May, G.,, F. Shaw,, H. Badrane, and, X. Vekemans. 1999. The signature of balancing selection: fungal mating compatibility gene evolution. Proc. Natl. Acad. Sci. USA 96:172177.
77. Müller, P.,, G. Weinzierl,, A. Brachmann,, M. Feldbrügge, and R. Kahmann. 2003. Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot. Cell 2:11871199.
78. Mutasa, E. S.,, A. M. Tymon,, B. Göttgens, F. M. Mellon,, P. F. R. Little, and, L. A. Casselton. 1989. Molecular organization of an A-mating type factor of the basidiomycete fungus Coprinus cinereus. Curr. Genet. 18:233229.
79. Olesnicky, N. S.,, A. J. Brown,, S. J. Dowell, and, L. A. Casselton. 1999. A constitutively active G-protein-coupled receptor causes mating self-incompatibility in the mushroom Coprinus. EMBO J. 18:27562763.
80. Olesnicky, N. S.,, A. J. Brown,, Y. Honda,, S. L. Dyas,, S. J. Dowell, and, L. A. Casselton. 2000. Self-compatible B mutants in Coprinus with altered pheromone-receptor specificities. Genetics 156:10251033.
81. O’Shea, S. F.,, P. T. Chaure,, J. R. Halsall,, N. S. Olesnicky,, A. Leibrandt,, 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 148:10811090.
82. Papazian, H. 1954. Exchange of incompatibility factors between the nuclei of a dikaryon. Science 119:691693.
83. Parag,, Y. 1962. Mutations in the B incompatibility factor of Schizophyllum commune. Proc. Natl. Acad. Sci. USA 48:743750.
84. Pardo, E. H.,, S. F. O’Shea, and L. A. Casselton. 1996. Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes. Genetics 148:8794.
85. Polak, E.,, R. Hermann,, U. Kües, and M. Aebi. 1997. Asexual development in Coprinus cinereus: structure and development of oidiophores and oidia in an Amut Bmut homokaryon. Fungal Genet. Biol. 22:112126.
86. Raper, C. A., and, J. R. Raper. 1973. Mutational analysis of a regulatory gene for morphogenesis in Schizophyllum. Proc. Natl. Acad. Sci. USA 70:14271431.
87. Raper, J. R. 1966. Genetics of Sexuality in Higher Fungi. Ronald Press, New York, NY.
88. Raper, J. R., and, M. Raudaskoski. 1968. Secondary mutations at the incompatibility locus of Schizophyllum. Heredity 23:109117.
89. Raper, J. R.,, M. G. Baxter, and, R. B. Middleton. 1958. The genetic structure of the incompatibility factors in Schizophyllum commune. Proc. Natl. Acad. Sci. USA 44:887900.
90. Raper, J. R.,, D. H. Boyd, and, C. A. Raper. 1965. Primary and secondary mutations at the incompatibility loci in Schizophyllum. Proc. Natl. Acad. Sci. USA 53:13241332.
91. Raudaskoski, M.,, J. Stamberg,, N. Bawnik, and, Y. Koltin. 1976. Mutational analysis of natural alleles at the B incompatibility factor of Schizophyllum commune: α2 and α6. Genetics 83:507516.
92. 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.
93. Scherer, M.,, K. Heimel,, V. Starke, and, J. Kämper. 2006. The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18:23882401.
94. 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.
95. Spellig, T.,, M. Bölker, F. Lottspeich,, R. W. Frank, and, R. Kahmann. 1994. Pheromones trigger filamentous growth in Ustilago maydis. EMBO J. 13:16201627.
96. Spit, A.,, R. H. Hyland,, E. J. C. Mellor, and, L. A. Casselton. 1998. A role for heterodimerization in nuclear localization of a homeodomain protein. Proc. Natl. Acad. Sci. USA 95:62286233.
97. Srivilai, P. 2006. Molecular Analysis of Genes Acting in Fruiting Body Development in Basidiomycetes. Ph.D. thesis. Georg-August-University Göttingen, Göttingen, Germany.
98. Stankis, M. M.,, C. A. Specht,, H. L. Yang,, L. Giasson,, R. C. Ullrich, and, C. P. Novotny. 1992. The mating type locus of Schizophyllum commune encodes two dissimilar multiallelic homeodomain proteins. Proc. Natl. Acad. Sci. USA 89:71607173.
99. 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.
100. Swiezynski, K. M., and, P. R. Day. 1960. Heterokaryon formation in Coprinus lagopus. Genet. Res. 1:114128.
101. Terashima, K.,, K. Yuki,, H. Maraguchi,, M. Akiyama, and, T. Kamada. 2005. The dst1 gene involved in mushroom photomorphogenesis of Coprinus cinereus encodes a putative photoreceptor for blue light. Genetics 171:101108.
102. Vaillancourt, L. J.,, M. Raudaskoski,, C. A. Specht, and, C. A. Raper. 1997. Multiple genes encoding pheromones and a pheromone receptor define the Bβ1 mating-type specificity in Schizophyllum commune. Genetics 146:541551.
103. Velagapudi, R. 2006. Extracellular Matrix Proteins in Growth and Fruiting Body Development of Straw and Wood Degrading Basidiomycetes. Ph.D. thesis. Georg-August-University Göttingen, Göttingen, Germany.
104. Wendland, J.,, L. J. Vaillancourt,, J. Hegner,, K. B. Lengeler,, K. J. Laddison,, C. A. Specht,, C. A. Raper, and, E. Kothe. 1995. The mating-type locus of Bα1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J. 14:52715278.
105. Yue, C. L.,, M. Osier,, C. P. Novotny, and, R. C. Ullrich. 1997. The specificity determinant of the Y mating-type proteins of Schizophyllum commune is also essential for Y-Z protein binding. Genetics 145:253260.
106. 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. 31:720.
107. Zhang, L.,, R. A. Baasiri, and, N. K. Van Alfen. 1998. Viral regulation of fungal pheromone precursor gene expression. Mol. Biol. Cell 18:953959.

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