Chapter 6 : Fungal Sex: The

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

Preview this chapter:
Zoom in

Fungal Sex: The , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap06-2.gif


There are ∼64,000 known species within the , making it the largest phylum of Fungi. Major subphyla include the (e.g., ), the (including and clades), and the (the largest subphylum, which includes the , , , and ) (see Fig. 1 ). Most grow as budding yeast or are dimorphic (can grow as yeast or filaments), whereas most are predominantly filamentous, although some are also dimorphic.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Phylogenetic relationships of major groups of fungi. Synthesis from references . Numbers at the nodes indicate estimated age, in millions of years, at which an ancestral group arose. Abbreviations: An, ; Ca, ; Ch, ; Fg, ; Pa, ; Nc, ; Sc, ; Sp, . Numbers in parentheses indicate the approximate age of that group in millions of years.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Life cycles of and . Both species can divide asexually or can undergo opposite sex mating. Meiosis and sporulation is used to complete the life cycle and regenerate haploid forms of the species.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Pheromone signaling in and . Pheromone signaling is transduced from a G-protein coupled receptor via a mitogen-activated protein kinase (MAPK) cascade into a transcriptional response in the nucleus. In , pheromone-receptor interactions cause dissociation of the G protein complex, and Gβγ subunits promote pheromone signaling via two scaffold proteins. The Ste5 scaffold mediates MAPK signaling and the transcriptional response to pheromone, whereas the Far1 scaffold interacts with Cdc42 to mediate shmoo formation and also leads to cell cycle arrest. In , no scaffold protein has been identified for pheromone signaling. Here, the Gα subunit transduces the pheromone signal to the MAPK cascade and does so in concert with Ste4 and Ras1 activities.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Images of ascomycetes undergoing sexual reproduction. The top row of images shows tetrads (four ascospores) produced by meiosis, dyads (two cell ascospores) produced by meiosis within the mating zygote, and a mating zygote with attached daughter cell buds. The bottom row of images shows a pseudothecium with extruded asci from the self-incompatible species , tetrads, and asci containing filamentous ascospores. Scale bars in the top three panels are 3.4 µm, 5 µm, and 8.5 µm, respectively. We acknowledge Aaron Neiman (Stony Brook University) and Matthew Hirakawa (Brown University) for the images of and cells, respectively.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Regulation of meiosis in and . In , two long noncoding RNAs, and , regulate the expression of and , respectively, thereby controlling entry into meiosis. In , Mei2 and the long noncoding RNA meiRNA play a central role in meiotic regulation by suppressing Mmi1 and thereby stabilizing mRNAs necessary for entry into meiosis.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Mating type cassettes in and . In both yeasts, mating type switching occurs by copying genetic information from a silent cassette into the transcriptionally active locus. In , silent cassettes are present at α and and are copied into the active locus. Recombination is activated by a DNA double-strand break introduced by the HO endonuclease at . A recombination enhancer (RE) promotes recombination between and α. In , silent cassettes are present at and and are copied into the active locus. Each cassette is flanked by homology regions (H1 and H2), and an imprinting event at H1 leads to recombinational repair of the damage using DNA from a silent cassette.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7
Figure 7

Mechanism of mating-type switching in . During mating-type switching, a DNA imprint is first introduced during lagging strand DNA replication at the locus. During the next round of DNA replication, the imprint is converted into a DNA double-strand break by leading strand synthesis. The DNA break initiates recombinational repair with one of the silent cassettes ( or ), resulting in switching of the cassette at the active locus.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 8
Figure 8

Evolution of mating type-switching mechanisms. In , mating-type switching occurs by a flip-flop inversion mechanism. Inverted repeat (IR) regions flank a transcriptionally active locus and a silenced locus, the latter being located close to the telomere (TEL). Recombination events between IR regions lead to a change in mating type. Model for how mating type switching evolved in the . Note that both and exhibit a similar inversion mechanism for mating-type switching. Adapted from reference .

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 9
Figure 9

Generalized life cycle of filamentous . impacts all stages indicated (see text). Heterothallic species, inner ring (solid); homothallic species, outer ring (dashed).

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 10
Figure 10

Organization of the locus in model (and ). Black lines, idiomorphs; rectangles, MAT proteins with signature domains. Domain type is indicated in the large box on the right. Note the diversity of locus organization but recurrent types of protein carried. organization in heterothallic and homothallic representatives of each large class of fungi. White boxes, idiomorph; black boxes, idiomorph. Genes and their direction of transcription are noted. See text for details.

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 11
Figure 11

Phylogenetic relationships among members of the HMG-box superfamily. Adapted from Fig. 3 of reference and Fig. 2 of reference . Note that the alpha 1 domain (α1) is an HMG protein. Colors: MATα_HMG, green; MATA_HMG, cream; SOX-TCF, brown; HMGB-UBF, light blue; MAT1-1-3 in MATA, orange; STE11 in MATA, purple. Other labels: Microsporidia MAT sex locus in HMGB-UBF (dark blue), (Zygomycota) sexM and sexP, (Glomeromycota) HMG proteins in MATA_HMG group. Abbreviations: An, ; Ca, ; Ch, ; Fg, ; Pa, ; Nc, ; Sc, ; Sp, ; Sm, .

Citation: Bennett R, Turgeon B. 2017. Fungal Sex: The , p 117-145. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0005-2016
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Goddard MR . 2016. Molecular evolution: sex accelerates adaptation. Nature 531 : 176 177.[PubMed] [CrossRef]
2. McDonald MJ,, Rice DP,, Desai MM . 2016. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531 : 233 236.[PubMed] [CrossRef]
3. Sipiczki M . 2000. Where does fission yeast sit on the tree of life? Genome Biol 1 : 1011.1 .4.[PubMed] [CrossRef]
4. Sipiczki M, . 2004. Fission yeast phylogenesis and evolution, p 431 443. In Egel R (ed), The Molecular Biology of Schizosaccharomyces pombe. Springer-Verlag, Heidelberg, Germany.[CrossRef]
5. Herskowitz I,, Rine J,, Strathern J, . 1992. Mating type determination and mating-type interconversion in Saccharomyces cerevisiae , p 583 657. In Pringle JR,, Jones EW,, Broach JR (ed), The Molecular and Cellular Biology of the Yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
6. Johnson AD . 1995. Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Genet Dev 5 : 552 558.[CrossRef]
7. Kelly M,, Burke J,, Smith M,, Klar A,, Beach D . 1988. Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7 : 1537 1547.[PubMed]
8. Imai Y,, Yamamoto M . 1994. The fission yeast mating pheromone P-factor: its molecular structure, gene structure, and ability to induce gene expression and G1 arrest in the mating partner. Genes Dev 8 : 328 338.[CrossRef]
9. Kitamura K,, Shimoda C . 1991. The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J 10 : 3743 3751.[PubMed]
10. Davey J . 1992. Mating pheromones of the fission yeast Schizosaccharomyces pombe: purification and structural characterization of M-factor and isolation and analysis of two genes encoding the pheromone. EMBO J 11 : 951 960.[PubMed]
11. Tanaka K,, Davey J,, Imai Y,, Yamamoto M . 1993. Schizosaccharomyces pombe map3+ encodes the putative M-factor receptor. Mol Cell Biol 13 : 80 88.[PubMed] [CrossRef]
12. Bardwell L . 2005. A walk-through of the yeast mating pheromone response pathway. Peptides 26 : 339 350.[CrossRef]
13. Chen RE,, Thorner J . 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae . Biochim Biophys Acta 1773 : 1311 1340.[PubMed] [CrossRef]
14. Jones SK Jr,, Bennett RJ . 2011. Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48 : 668 676.[PubMed] [CrossRef]
15. Merlini L,, Dudin O,, Martin SG . 2013. Mate and fuse: how yeast cells do it. Open Biol 3 : 130008.[PubMed] [CrossRef]
16. Butty AC,, Pryciak PM,, Huang LS,, Herskowitz I,, Peter M . 1998. The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating. Science 282 : 1511 1516.[PubMed] [CrossRef]
17. Leeuw T,, Wu C,, Schrag JD,, Whiteway M,, Thomas DY,, Leberer E . 1998. Interaction of a G-protein beta-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 391 : 191 195.[PubMed] [CrossRef]
18. Nern A,, Arkowitz RA . 1998. A GTP-exchange factor required for cell orientation. Nature 391 : 195 198.[PubMed] [CrossRef]
19. Whiteway MS,, Wu C,, Leeuw T,, Clark K,, Fourest-Lieuvin A,, Thomas DY,, Leberer E . 1995. Association of the yeast pheromone response G protein beta gamma subunits with the MAP kinase scaffold Ste5p. Science 269 : 1572 1575.[CrossRef]
20. Peter M,, Neiman AM,, Park HO,, van Lohuizen M,, Herskowitz I . 1996. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J 15 : 7046 7059.[PubMed]
21. Wang Y,, Chen W,, Simpson DM,, Elion EA . 2005. Cdc24 regulates nuclear shuttling and recruitment of the Ste5 scaffold to a heterotrimeric G protein in Saccharomyces cerevisiae . J Biol Chem 280 : 13084 13096.[PubMed] [CrossRef]
22. Peter M,, Gartner A,, Horecka J,, Ammerer G,, Herskowitz I . 1993. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73 : 747 760.[CrossRef] [PubMed]
23. Valtz N,, Peter M,, Herskowitz I . 1995. FAR1 is required for oriented polarization of yeast cells in response to mating pheromones. J Cell Biol 131 : 863 873.[PubMed] [CrossRef]
24. Choi KY,, Satterberg B,, Lyons DM,, Elion EA . 1994. Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae . Cell 78 : 499 512.[CrossRef] [PubMed]
25. Marcus S,, Polverino A,, Barr M,, Wigler M . 1994. Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module. Proc Natl Acad Sci USA 91 : 7762 7766.[PubMed] [CrossRef]
26. Printen JA,, Sprague GF Jr . 1994. Protein-protein interactions in the yeast pheromone response pathway: Ste5p interacts with all members of the MAP kinase cascade. Genetics 138 : 609 619.[PubMed]
27. Mahanty SK,, Wang Y,, Farley FW,, Elion EA . 1999. Nuclear shuttling of yeast scaffold Ste5 is required for its recruitment to the plasma membrane and activation of the mating MAPK cascade. Cell 98 : 501 512.[PubMed] [CrossRef]
28. Pryciak PM,, Huntress FA . 1998. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gbetagamma complex underlies activation of the yeast pheromone response pathway. Genes Dev 12 : 2684 2697.[CrossRef]
29. Wu C,, Leberer E,, Thomas DY,, Whiteway M . 1999. Functional characterization of the interaction of Ste50p with Ste11p MAPKKK in Saccharomyces cerevisiae . Mol Biol Cell 10 : 2425 2440.[PubMed] [CrossRef]
30. Good M,, Tang G,, Singleton J,, Reményi A,, Lim WA . 2009. The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136 : 1085 1097.[PubMed] [CrossRef]
31. Bardwell L,, Cook JG,, Zhu-Shimoni JX,, Voora D,, Thorner J . 1998. Differential regulation of transcription: repression by unactivated mitogen-activated protein kinase Kss1 requires the Dig1 and Dig2 proteins. Proc Natl Acad Sci USA 95 : 15400 15405.[CrossRef]
32. Olson KA,, Nelson C,, Tai G,, Hung W,, Yong C,, Astell C,, Sadowski I . 2000. Two regulators of Ste12p inhibit pheromone-responsive transcription by separate mechanisms. Mol Cell Biol 20 : 4199 4209.[PubMed] [CrossRef]
33. Dolan JW,, Kirkman C,, Fields S . 1989. The yeast STE12 protein binds to the DNA sequence mediating pheromone induction. Proc Natl Acad Sci USA 86 : 5703 5707.[CrossRef]
34. Errede B,, Ammerer G . 1989. STE12, a protein involved in cell-type-specific transcription and signal transduction in yeast, is part of protein-DNA complexes. Genes Dev 3 : 1349 1361.[CrossRef]
35. Sengupta P,, Cochran BH . 1990. The PRE and PQ box are functionally distinct yeast pheromone response elements. Mol Cell Biol 10 : 6809 6812.[PubMed] [CrossRef]
36. Sengupta P,, Cochran BH . 1991. MAT alpha 1 can mediate gene activation by a-mating factor. Genes Dev 5 : 1924 1934.[PubMed] [CrossRef]
37. Yuan YO,, Stroke IL,, Fields S . 1993. Coupling of cell identity to signal response in yeast: interaction between the alpha 1 and STE12 proteins. Genes Dev 7 : 1584 1597.[PubMed] [CrossRef]
38. Chou S,, Lane S,, Liu H . 2006. Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae . Mol Cell Biol 26 : 4794 4805.[PubMed] [CrossRef]
39. Elion EA,, Satterberg B,, Kranz JE . 1993. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol Biol Cell 4 : 495 510.[CrossRef]
40. Pope PA,, Bhaduri S,, Pryciak PM . 2014. Regulation of cyclin-substrate docking by a G1 arrest signaling pathway and the Cdk inhibitor Far1. Curr Biol 24 : 1390 1396.[PubMed] [CrossRef]
41. Nern A,, Arkowitz RAA . 1999. A Cdc24p-Far1p-Gbetagamma protein complex required for yeast orientation during mating. J Cell Biol 144 : 1187 1202.[CrossRef]
42. Matheos D,, Metodiev M,, Muller E,, Stone D,, Rose MD . 2004. Pheromone-induced polarization is dependent on the Fus3p MAPK acting through the formin Bni1p. J Cell Biol 165 : 99 109.[PubMed] [CrossRef]
43. Errede B,, Vered L,, Ford E,, Pena MI,, Elston TC . 2015. Pheromone-induced morphogenesis and gradient tracking are dependent on the MAPK Fus3 binding to Gα. Mol Biol Cell 26 : 3343 3358.[PubMed] [CrossRef]
44. Obara T,, Nakafuku M,, Yamamoto M,, Kaziro Y . 1991. Isolation and characterization of a gene encoding a G-protein alpha subunit from Schizosaccharomyces pombe: involvement in mating and sporulation pathways. Proc Natl Acad Sci USA 88 : 5877 5881.[PubMed] [CrossRef]
45. Navarro-Olmos R,, Kawasaki L,, Domínguez-Ramírez L,, Ongay-Larios L,, Pérez-Molina R,, Coria R . 2010. The beta subunit of the heterotrimeric G protein triggers the Kluyveromyces lactis pheromone response pathway in the absence of the gamma subunit. Mol Biol Cell 21 : 489 498.[CrossRef]
46. Dignard D,, André D,, Whiteway M . 2008. Heterotrimeric G-protein subunit function in Candida albicans: both the alpha and beta subunits of the pheromone response G protein are required for mating. Eukaryot Cell 7 : 1591 1599.[CrossRef]
47. Nadin-Davis SA,, Nasim A . 1990. Schizosaccharomyces pombe ras1 and byr1 are functionally related genes of the ste family that affect starvation-induced transcription of mating-type genes. Mol Cell Biol 10 : 549 560.[CrossRef]
48. Wang Y,, Xu HP,, Riggs M,, Rodgers L,, Wigler M . 1991. byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the ras1 mutant phenotype. Mol Cell Biol 11 : 3554 3563.[PubMed] [CrossRef]
49. Neiman AM,, Stevenson BJ,, Xu HP,, Sprague GF Jr,, Herskowitz I,, Wigler M,, Marcus S . 1993. Functional homology of protein kinases required for sexual differentiation in Schizosaccharomyces pombe and Saccharomyces cerevisiae suggests a conserved signal transduction module in eukaryotic organisms. Mol Biol Cell 4 : 107 120.[PubMed] [CrossRef]
50. Kjaerulff S,, Lautrup-Larsen I,, Truelsen S,, Pedersen M,, Nielsen O . 2005. Constitutive activation of the fission yeast pheromone-responsive pathway induces ectopic meiosis and reveals Ste11 as a mitogen-activated protein kinase target. Mol Cell Biol 25 : 2045 2059.[PubMed] [CrossRef]
51. Barr MM,, Tu H,, Van Aelst L,, Wigler M . 1996. Identification of Ste4 as a potential regulator of Byr2 in the sexual response pathway of Schizosaccharomyces pombe . Mol Cell Biol 16 : 5597 5603.[PubMed] [CrossRef]
52. Ramachander R,, Kim CA,, Phillips ML,, Mackereth CD,, Thanos CD,, McIntosh LP,, Bowie JU . 2002. Oligomerization-dependent association of the SAM domains from Schizosaccharomyces pombe Byr2 and Ste4. J Biol Chem 277 : 39585 39593.[PubMed] [CrossRef]
53. Masuda T,, Kariya K,, Shinkai M,, Okada T,, Kataoka T . 1995. Protein kinase Byr2 is a target of Ras1 in the fission yeast Schizosaccharomyces pombe . J Biol Chem 270 : 1979 1982.[PubMed] [CrossRef]
54. Papadaki P,, Pizon V,, Onken B,, Chang EC . 2002. Two ras pathways in fission yeast are differentially regulated by two ras guanine nucleotide exchange factors. Mol Cell Biol 22 : 4598 4606.[PubMed] [CrossRef]
55. Mochizuki N,, Yamamoto M . 1992. Reduction in the intracellular cAMP level triggers initiation of sexual development in fission yeast. Mol Gen Genet 233 : 17 24.[PubMed] [CrossRef]
56. Schwartz MA,, Madhani HD . 2004. Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae . Annu Rev Genet 38 : 725 748.[PubMed] [CrossRef]
57. Saito H . 2010. Regulation of cross-talk in yeast MAPK signaling pathways. Curr Opin Microbiol 13 : 677 683.[PubMed] [CrossRef]
58. Bardwell L . 2006. Mechanisms of MAPK signalling specificity. Biochem Soc Trans 34 : 837 841.[PubMed] [CrossRef]
59. Kassir Y,, Granot D,, Simchen G . 1988. IME1, a positive regulator gene of meiosis in S. cerevisiae . Cell 52 : 853 862.[PubMed] [CrossRef]
60. van Werven FJ,, Amon A . 2011. Regulation of entry into gametogenesis. Philos Trans R Soc Lond B Biol Sci 366 : 3521 3531.[PubMed] [CrossRef]
61. van Werven FJ,, Neuert G,, Hendrick N,, Lardenois A,, Buratowski S,, van Oudenaarden A,, Primig M,, Amon A . 2012. Transcription of two long noncoding RNAs mediates mating-type control of gametogenesis in budding yeast. Cell 150 : 1170 1181.[PubMed] [CrossRef]
62. Shah JC,, Clancy MJ . 1992. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae . Mol Cell Biol 12 : 1078 1086.[PubMed] [CrossRef]
63. Clancy MJ,, Shambaugh ME,, Timpte CS,, Bokar JA . 2002. Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6-methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucleic Acids Res 30 : 4509 4518.[PubMed] [CrossRef]
64. Hongay CF,, Grisafi PL,, Galitski T,, Fink GR . 2006. Antisense transcription controls cell fate in Saccharomyces cerevisiae . Cell 127 : 735 745.[PubMed] [CrossRef]
65. Gelfand B,, Mead J,, Bruning A,, Apostolopoulos N,, Tadigotla V,, Nagaraj V,, Sengupta AM,, Vershon AK . 2011. Regulated antisense transcription controls expression of cell-type-specific genes in yeast. Mol Cell Biol 31 : 1701 1709.[CrossRef]
66. Chu S,, Herskowitz I . 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1 : 685 696.[PubMed] [CrossRef]
67. Primig M,, Williams RM,, Winzeler EA,, Tevzadze GG,, Conway AR,, Hwang SY,, Davis RW,, Esposito RE . 2000. The core meiotic transcriptome in budding yeasts. Nat Genet 26 : 415 423.[PubMed] [CrossRef]
68. Winter E . 2012. The Sum1/Ndt80 transcriptional switch and commitment to meiosis in Saccharomyces cerevisiae . Microbiol Mol Biol Rev 76 : 1 15.[PubMed] [CrossRef]
69. Mitchell AP . 1994. Control of meiotic gene expression in Saccharomyces cerevisiae . Microbiol Rev 58 : 56 70.[PubMed]
70. Rubin-Bejerano I,, Mandel S,, Robzyk K,, Kassir Y . 1996. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol Cell Biol 16 : 2518 2526.[CrossRef]
71. Washburn BK,, Esposito RE . 2001. Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol Cell Biol 21 : 2057 2069.[PubMed] [CrossRef]
72. Mallory MJ,, Cooper KF,, Strich R . 2007. Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol Cell 27 : 951 961.[PubMed] [CrossRef]
73. Mitchell AP,, Driscoll SE,, Smith HE . 1990. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae . Mol Cell Biol 10 : 2104 2110.[PubMed] [CrossRef]
74. Guttmann-Raviv N,, Martin S,, Kassir Y . 2002. Ime2, a meiosis-specific kinase in yeast, is required for destabilization of its transcriptional activator, Ime1. Mol Cell Biol 22 : 2047 2056.[PubMed] [CrossRef]
75. Pierce M,, Benjamin KR,, Montano SP,, Georgiadis MM,, Winter E,, Vershon AK . 2003. Sum1 and Ndt80 proteins compete for binding to middle sporulation element sequences that control meiotic gene expression. Mol Cell Biol 23 : 4814 4825.[CrossRef]
76. Tsuchiya D,, Yang Y,, Lacefield S . 2014. Positive feedback of NDT80 expression ensures irreversible meiotic commitment in budding yeast. PLoS Genet 10 : e1004398.[CrossRef]
77. Willer M,, Hoffmann L,, Styrkársdóttir U,, Egel R,, Davey J,, Nielsen O . 1995. Two-step activation of meiosis by the mat1 locus in Schizosaccharomyces pombe . Mol Cell Biol 15 : 4964 4970.[PubMed] [CrossRef]
78. van Heeckeren WJ,, Dorris DR,, Struhl K . 1998. The mating-type proteins of fission yeast induce meiosis by directly activating mei3 transcription. Mol Cell Biol 18 : 7317 7326.[PubMed] [CrossRef]
79. McLeod M,, Stein M,, Beach D . 1987. The product of the mei3+ gene, expressed under control of the mating-type locus, induces meiosis and sporulation in fission yeast. EMBO J 6 : 729 736.[PubMed]
80. Harigaya Y,, Tanaka H,, Yamanaka S,, Tanaka K,, Watanabe Y,, Tsutsumi C,, Chikashige Y,, Hiraoka Y,, Yamashita A,, Yamamoto M . 2006. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442 : 45 50.[PubMed] [CrossRef]
81. Yamashita A,, Shichino Y,, Tanaka H,, Hiriart E,, Touat-Todeschini L,, Vavasseur A,, Ding DQ,, Hiraoka Y,, Verdel A,, Yamamoto M . 2012. Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes. Open Biol 2 : 120014.[CrossRef]
82. Yamamoto M . 2010. The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast. Proc Jpn Acad Ser B Phys Biol Sci 86 : 788 797.[PubMed] [CrossRef]
83. Mata J,, Wilbrey A,, Bähler J . 2007. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol 8 : R217.[PubMed] [CrossRef]
84. McLeod M,, Beach D . 1988. A specific inhibitor of the ran1+ protein kinase regulates entry into meiosis in Schizosaccharomyces pombe . Nature 332 : 509 514.[CrossRef]
85. Li P,, McLeod M . 1996. Molecular mimicry in development: identification of ste11+ as a substrate and mei3+ as a pseudosubstrate inhibitor of ran1+ kinase. Cell 87 : 869 880.[PubMed] [CrossRef]
86. Sugimoto A,, Iino Y,, Maeda T,, Watanabe Y,, Yamamoto M . 1991. Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev 5 : 1990 1999.[CrossRef]
87. Haber JE . 2012. Mating-type genes and MAT switching in Saccharomyces cerevisiae . Genetics 191 : 33 64.[PubMed] [CrossRef]
88. Sil A,, Herskowitz I . 1996. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell 84 : 711 722.[CrossRef] [PubMed]
89. Long RM,, Singer RH,, Meng X,, Gonzalez I,, Nasmyth K,, Jansen RP . 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277 : 383 387.[PubMed] [CrossRef]
90. Paquin N,, Chartrand P . 2008. Local regulation of mRNA translation: new insights from the bud. Trends Cell Biol 18 : 105 111.[PubMed] [CrossRef]
91. Niedner A,, Edelmann FT,, Niessing D . 2014. Of social molecules: the interactive assembly of ASH1 mRNA-transport complexes in yeast. RNA Biol 11 : 998 1009.[PubMed] [CrossRef]
92. Koufopanou V,, Burt A . 2005. Degeneration and domestication of a selfish gene in yeast: molecular evolution versus site-directed mutagenesis. Mol Biol Evol 22 : 1535 1538.[PubMed] [CrossRef]
93. Klar AJ,, Hicks JB,, Strathern JN . 1982. Directionality of yeast mating-type interconversion. Cell 28 : 551 561.[PubMed] [CrossRef]
94. Weiler KS,, Broach JR . 1992. Donor locus selection during Saccharomyces cerevisiae mating type interconversion responds to distant regulatory signals. Genetics 132 : 929 942.[PubMed]
95. Wu X,, Haber JE . 1995. MAT a donor preference in yeast mating-type switching: activation of a large chromosomal region for recombination. Genes Dev 9 : 1922 1932.[CrossRef]
96. Wu X,, Moore JK,, Haber JE . 1996. Mechanism of MAT alpha donor preference during mating-type switching of Saccharomyces cerevisiae . Mol Cell Biol 16 : 657 668.[PubMed] [CrossRef]
97. Wu C,, Weiss K,, Yang C,, Harris MA,, Tye BK,, Newlon CS,, Simpson RT,, Haber JE . 1998. Mcm1 regulates donor preference controlled by the recombination enhancer in Saccharomyces mating-type switching. Genes Dev 12 : 1726 1737.[CrossRef]
98. Wu X,, Haber JEA . 1996. A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell 87 : 277 285.[CrossRef]
99. Li J,, Coïc E,, Lee K,, Lee CS,, Kim JA,, Wu Q,, Haber JE . 2012. Regulation of budding yeast mating-type switching donor preference by the FHA domain of Fkh1. PLoS Genet 8 : e1002630.[PubMed] [CrossRef]
100. Sun K,, Coïc E,, Zhou Z,, Durrens P,, Haber JE . 2002. Saccharomyces forkhead protein Fkh1 regulates donor preference during mating-type switching through the recombination enhancer. Genes Dev 16 : 2085 2096.[CrossRef]
101. Klar AJ . 1987. Differentiated parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature 326 : 466 470.[CrossRef]
102. Klar AJ . 1990. The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. EMBO J 9 : 1407 1415.[PubMed]
103. Dalgaard JZ,, Klar AJ . 1999. Orientation of DNA replication establishes mating-type switching pattern in S. pombe . Nature 400 : 181 184.[PubMed] [CrossRef]
104. Klar AJ,, Ishikawa K,, Moore S . 2014. A unique DNA recombination mechanism of the mating/cell-type switching of fission yeasts: a review. Microbiol Spectr 2( 5) : MDNA3-0003-2014.[CrossRef]
105. Vengrova S,, Dalgaard JZ . 2006. The wild-type Schizosaccharomyces pombe mat1 imprint consists of two ribonucleotides. EMBO Rep 7 : 59 65.[PubMed] [CrossRef]
106. Thon G,, Klar AJ . 1993. Directionality of fission yeast mating-type interconversion is controlled by the location of the donor loci. Genetics 134 : 1045 1054.[PubMed]
107. Jakočiūnas T,, Holm LR,, Verhein-Hansen J,, Trusina A,, Thon G . 2013. Two portable recombination enhancers direct donor choice in fission yeast heterochromatin. PLoS Genet 9 : e1003762.[CrossRef]
108. Yu C,, Bonaduce MJ,, Klar AJ . 2012. Going in the right direction: mating-type switching of Schizosaccharomyces pombe is controlled by judicious expression of two different swi2 transcripts. Genetics 190 : 977 987.[PubMed] [CrossRef]
109. Knop M . 2006. Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding. BioEssays 28 : 696 708.[PubMed] [CrossRef]
110. Gordon JL,, Armisén D,, Proux-Wéra E,, ÓhÉigeartaigh SS,, Byrne KP,, Wolfe KH . 2011. Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. Proc Natl Acad Sci USA 108 : 20024 20029.[CrossRef]
111. Hanson SJ,, Byrne KP,, Wolfe KH . 2014. Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locus Saccharomyces cerevisiae system. Proc Natl Acad Sci USA 111 : E4851 E4858.[CrossRef]
112. Maekawa H,, Kaneko Y . 2014. Inversion of the chromosomal region between two mating type loci switches the mating type in Hansenula polymorpha . PLoS Genet 10 : e1004796.[PubMed] [CrossRef]
113. Butler G,, Rasmussen MD,, Lin MF,, Santos MA,, Sakthikumar S,, Munro CA,, Rheinbay E,, Grabherr M,, Forche A,, Reedy JL,, Agrafioti I,, Arnaud MB,, Bates S,, Brown AJ,, Brunke S,, Costanzo MC,, Fitzpatrick DA,, de Groot PW,, Harris D,, Hoyer LL,, Hube B,, Klis FM,, Kodira C,, Lennard N,, Logue ME,, Martin R,, Neiman AM,, Nikolaou E,, Quail MA,, Quinn J,, Santos MC,, Schmitzberger FF,, Sherlock G,, Shah P,, Silverstein KA,, Skrzypek MS,, Soll D,, Staggs R,, Stansfield I,, Stumpf MP,, Sudbery PE,, Srikantha T,, Zeng Q,, Berman J,, Berriman M,, Heitman J,, Gow NA,, Lorenz MC,, Birren BW,, Kellis M,, Cuomo CA . 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459 : 657 662.[CrossRef]
114. Butler G . 2010. Fungal sex and pathogenesis. Clin Microbiol Rev 23 : 140 159.[PubMed] [CrossRef]
115. Alby K,, Bennett RJ . 2010. Sexual reproduction in the Candida clade: cryptic cycles, diverse mechanisms, and alternative functions. Cell Mol Life Sci 67 : 3275 3285.[PubMed] [CrossRef]
116. Reedy JL,, Floyd AM,, Heitman J . 2009. Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19 : 891 899.[PubMed] [CrossRef]
117. Sherwood RK,, Scaduto CM,, Torres SE,, Bennett RJ . 2014. Convergent evolution of a fused sexual cycle promotes the haploid lifestyle. Nature 506 : 387 390.[CrossRef]
118. Young LY,, Lorenz MC,, Heitman J . 2000. A STE12 homolog is required for mating but dispensable for filamentation in Candida lusitaniae . Genetics 155 : 17 29.[PubMed]
119. Pfaller MA,, Diekema DJ . 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20 : 133 163.[PubMed] [CrossRef]
120. Ghannoum MA,, Jurevic RJ,, Mukherjee PK,, Cui F,, Sikaroodi M,, Naqvi A,, Gillevet PM . 2010. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6 : e1000713.[PubMed] [CrossRef]
121. Hull CM,, Johnson AD . 1999. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans . Science 285 : 1271 1275.[PubMed] [CrossRef]
122. Hull CM,, Raisner RM,, Johnson AD . 2000. Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science 289 : 307 310.[PubMed] [CrossRef]
123. Magee BB,, Magee PT . 2000. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289 : 310 313.[PubMed] [CrossRef]
124. Miller MG,, Johnson AD . 2002. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110 : 293 302.[PubMed] [CrossRef]
125. Porman AM,, Alby K,, Hirakawa MP,, Bennett RJ . 2011. Discovery of a phenotypic switch regulating sexual mating in the opportunistic fungal pathogen Candida tropicalis . Proc Natl Acad Sci USA 108 : 21158 21163.[CrossRef]
126. Puel A,, Cypowyj S,, Bustamante J,, Wright JF,, Liu L,, Lim HK,, Migaud M,, Israel L,, Chrabieh M,, Audry M,, Gumbleton M,, Toulon A,, Bodemer C,, El-Baghdadi J,, Whitters M,, Paradis T,, Brooks J,, Collins M,, Wolfman NM,, Al-Muhsen S,, Galicchio M,, Abel L,, Picard C,, Casanova JL . 2011. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332 : 65 68.[PubMed] [CrossRef]
127. Xie J,, Du H,, Guan G,, Tong Y,, Kourkoumpetis TK,, Zhang L,, Bai FY,, Huang G . 2012. N-acetylglucosamine induces white-to-opaque switching and mating in Candida tropicalis, providing new insights into adaptation and fungal sexual evolution. Eukaryot Cell 11 : 773 782.[PubMed] [CrossRef]
128. Lohse MB,, Johnson AD . 2009. White-opaque switching in Candida albicans . Curr Opin Microbiol 12 : 650 654.[PubMed] [CrossRef]
129. Soll DR . 2009. Why does Candida albicans switch? FEMS Yeast Res 9 : 973 989.[PubMed] [CrossRef]
130. Morschhäuser J . 2010. Regulation of white-opaque switching in Candida albicans . Med Microbiol Immunol (Berl) 199 : 165 172.[PubMed] [CrossRef]
131. Scaduto CM,, Bennett RJ . 2015. Candida albicans the chameleon: transitions and interactions between multiple phenotypic states confer phenotypic plasticity. Curr Opin Microbiol 26 : 102 108.[PubMed] [CrossRef]
132. Si H,, Hernday AD,, Hirakawa MP,, Johnson AD,, Bennett RJ . 2013. Candida albicans white and opaque cells undergo distinct programs of filamentous growth. PLoS Pathog 9 : e1003210.[PubMed] [CrossRef]
133. Kolotila MP,, Diamond RD . 1990. Effects of neutrophils and in vitro oxidants on survival and phenotypic switching of Candida albicans WO-1. Infect Immun 58 : 1174 1179.[PubMed]
134. Lohse MB,, Johnson AD . 2008. Differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS One 3 : e1473.[CrossRef]
135. Kvaal CA,, Srikantha T,, Soll DR . 1997. Misexpression of the white-phase-specific gene WH11 in the opaque phase of Candida albicans affects switching and virulence. Infect Immun 65 : 4468 4475.[PubMed]
136. Johnson A . 2003. The biology of mating in Candida albicans . Nat Rev Microbiol 1 : 106 116.[PubMed] [CrossRef]
137. Lachke SA,, Lockhart SR,, Daniels KJ,, Soll DR . 2003. Skin facilitates Candida albicans mating. Infect Immun 71 : 4970 4976.[PubMed] [CrossRef]
138. Rikkerink EH,, Magee BB,, Magee PT . 1988. Opaque-white phenotype transition: a programmed morphological transition in Candida albicans . J Bacteriol 170 : 895 899.[PubMed]
139. Daniels KJ,, Srikantha T,, Lockhart SR,, Pujol C,, Soll DR . 2006. Opaque cells signal white cells to form biofilms in Candida albicans . EMBO J 25 : 2240 2252.[PubMed] [CrossRef]
140. Park YN,, Daniels KJ,, Pujol C,, Srikantha T,, Soll DR . 2013. Candida albicans forms a specialized “sexual” as well as “pathogenic” biofilm. Eukaryot Cell 12 : 1120 1131.[PubMed] [CrossRef]
141. Côte P,, Sulea T,, Dignard D,, Wu C,, Whiteway M . 2011. Evolutionary reshaping of fungal mating pathway scaffold proteins. MBio 2 : e00230-10.[PubMed] [CrossRef]
142. Côte P,, Whiteway M . 2008. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol Microbiol 68 : 392 404.[PubMed] [CrossRef]
143. Sai S,, Holland LM,, McGee CF,, Lynch DB,, Butler G . 2011. Evolution of mating within the Candida parapsilosis species group. Eukaryot Cell 10 : 578 587.[PubMed] [CrossRef]
144. Pryszcz LP,, Németh T,, Gácser A,, Gabaldón T . 2013. Unexpected genomic variability in clinical and environmental strains of the pathogenic yeast Candida parapsilosis . Genome Biol Evol 5 : 2382 2392.[PubMed] [CrossRef]
145. Pryszcz LP,, Németh T,, Saus E,, Ksiezopolska E,, Hegedűsová E,, Nosek J,, Wolfe KH,, Gacser A,, Gabaldón T . 2015. The genomic aftermath of hybridization in the opportunistic pathogen Candida metapsilosis . PLoS Genet 11 : e1005626.[CrossRef]
146. Pryszcz LP,, Németh T,, Gácser A,, Gabaldón T . 2014. Genome comparison of Candida orthopsilosis clinical strains reveals the existence of hybrids between two distinct subspecies. Genome Biol Evol 6 : 1069 1078.[CrossRef]
147. Tsong AE,, Tuch BB,, Li H,, Johnson AD . 2006. Evolution of alternative transcriptional circuits with identical logic. Nature 443 : 415 420.[PubMed] [CrossRef]
148. Tsong AE,, Miller MG,, Raisner RM,, Johnson AD . 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115 : 389 399.[PubMed] [CrossRef]
149. Baker CR,, Booth LN,, Sorrells TR,, Johnson AD . 2012. Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. Cell 151 : 80 95.[PubMed] [CrossRef]
150. Butler G,, Kenny C,, Fagan A,, Kurischko C,, Gaillardin C,, Wolfe KH . 2004. Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Natl Acad Sci USA 101 : 1632 1637.[PubMed] [CrossRef]
151. Forche A,, Alby K,, Schaefer D,, Johnson AD,, Berman J,, Bennett RJ . 2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6 : e110.[CrossRef]
152. Bennett RJ,, Uhl MA,, Miller MG,, Johnson AD . 2003. Identification and characterization of a Candida albicans mating pheromone. Mol Cell Biol 23 : 8189 8201.[PubMed] [CrossRef]
153. Hickman MA,, Paulson C,, Dudley A,, Berman J . 2015. Parasexual ploidy reduction drives population heterogeneity through random and transient aneuploidy in Candida albicans . Genetics 200 : 781 794.[PubMed] [CrossRef]
154. Hickman MA,, Zeng G,, Forche A,, Hirakawa MP,, Abbey D,, Harrison BD,, Wang YM,, Su CH,, Bennett RJ,, Wang Y,, Berman J . 2013. The ‘obligate diploid’ Candida albicans forms mating-competent haploids. Nature 494 : 55 59.[CrossRef]
155. Alby K,, Schaefer D,, Bennett RJ . 2009. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans . Nature 460 : 890 893.[PubMed] [CrossRef]
156. Alby K,, Bennett RJ . 2011. Interspecies pheromone signaling promotes biofilm formation and same-sex mating in Candida albicans . Proc Natl Acad Sci USA 108 : 2510 2515.[PubMed] [CrossRef]
157. Fabre E,, Muller H,, Therizols P,, Lafontaine I,, Dujon B,, Fairhead C . 2005. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol Biol Evol 22 : 856 873.[PubMed] [CrossRef]
158. Debuchy R,, Turgeon BG, . 2006. Mating-type structure, evolution and function in Euascomycetes , p 293 323. In Kües U,, Fischer R (ed), The Mycota. Growth, Differentiation and Sexuality. 1. Springer-Verlag, Berlin, Germany.[CrossRef]
159. Debuchy R,, Berteaux-Lecellier V,, Silar P, . 2010. Mating systems and sexual morphogenesis in Ascomycetes , p 501 535. In Borkovich K,, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC.[CrossRef]
160. Raju NB . 1980. Meiosis and ascospore genesis in Neurospora . Eur J Cell Biol 23 : 208 223.[PubMed]
161. Trail F,, Common R . 2000. Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92 : 130 138.[CrossRef]
162. Butler G, . 2007. The evolution of MAT: the Ascomycetes , p 3 18. In Heitman J,, Kronstad JW,, Taylor JW,, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC.[CrossRef]
163. Turgeon B,, Debuchy R, . 2007. Cochliobolus and Podospora: mechanisms of sex determination and the evolution of reproductive lifestyle, p 93 121. In Heitman J,, Kronstad JW,, Taylor JW,, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC.[CrossRef]
164. Glass NL,, Grotelueschen J,, Metzenberg RL . 1990. Neurospora crassa A mating-type region. Proc Natl Acad Sci USA 87 : 4912 4916.[PubMed] [CrossRef]
165. Staben C . 1996. The mating-type locus of Neurospora crassa . J Genet 75 : 341 350.[CrossRef]
166. Turgeon BG,, Ciuffetti L,, Schafer W,, Yoder OC, . 1988. Isolation of the mating type locus of Cochliobolus heterostrophus , p 265 266. In Palacios R,, Verma DPS (ed), Molecular Genetics of Plant-Microbe Interactions. APS Press, St Paul, MN.
167. Debuchy R,, Coppin E . 1992. The mating types of Podospora anserina: functional analysis and sequence of the fertilization domains. Mol Gen Genet 233 : 113 121.[PubMed] [CrossRef]
168. Turgeon BG,, Yoder OC . 2000. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31 : 1 5.[PubMed] [CrossRef]
169. Metzenberg RL,, Glass NL . 1990. Mating type and mating strategies in Neurospora . BioEssays 12 : 53 59.[PubMed] [CrossRef]
170. Glass NL,, Staben C . 1990. Genetic control of mating in Neurospora crassa . Semin Dev Biol 1 : 177 184.
171. Glass NL,, Staben C . 1997. Neurospora mating type symbol mt revised to mat . Fungal Genet Newsl 44 : 64.
172. Debuchy R,, Arnaise S,, Lecellier G . 1993. The mat- allele of Podospora anserina contains three regulatory genes required for the development of fertilized female organs. Mol Gen Genet 241 : 667 673.[CrossRef]
173. Sugimoto A,, Iino Y,, Maeda T,, Watanabe Y,, Yamamoto M . 1991. Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev 5 : 1990 1999.[CrossRef]
174. Herskowitz I . 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342 : 749 757.[PubMed] [CrossRef]
175. Turgeon BG,, Bohlmann H,, Ciuffetti LM,, Christiansen SK,, Yang G,, Schäfer W,, Yoder OC . 1993. Cloning and analysis of the mating type genes from Cochliobolus heterostrophus . Mol Gen Genet 238 : 270 284.[PubMed]
176. Mandel MA,, Barker BM,, Kroken S,, Rounsley SD,, Orbach MJ . 2007. Genomic and population analyses of the mating type loci in Coccidioides species reveal evidence for sexual reproduction and gene acquisition. Eukaryot Cell 6 : 1189 1199.[CrossRef]
177. Galagan JE,, Calvo SE,, Cuomo C,, Ma LJ,, Wortman JR,, Batzoglou S,, Lee SI,, Baştürkmen M,, Spevak CC,, Clutterbuck J,, Kapitonov V,, Jurka J,, Scazzocchio C,, Farman M,, Butler J,, Purcell S,, Harris S,, Braus GH,, Draht O,, Busch S,, D’Enfert C,, Bouchier C,, Goldman GH,, Bell-Pedersen D,, Griffiths-Jones S,, Doonan JH,, Yu J,, Vienken K,, Pain A,, Freitag M,, Selker EU,, Archer DB,, Peñalva MA,, Oakley BR,, Momany M,, Tanaka T,, Kumagai T,, Asai K,, Machida M,, Nierman WC,, Denning DW,, Caddick M,, Hynes M,, Paoletti M,, Fischer R,, Miller B,, Dyer P,, Sachs MS,, Osmani SA,, Birren BW . 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae . Nature 438 : 1105 1115.[CrossRef]
178. Pöggeler S,, Risch S,, Kück U,, Osiewacz HD . 1997. Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147 : 567 580.[PubMed]
179. Dyer PS,, Bowyer P,, Lucas JA,, Peberdy JF . 1997. Cloning of a putative mating-type gene from the Discomycete fungus Tapesia yallundae , p 49. In Proceedings of the 19th Fungal Genetics Conference, Pacific Grove, CA.
180. Chitrampalam P,, Inderbitzin P,, Maruthachalam K,, Wu BM,, Subbarao KV . 2013. The Sclerotinia sclerotiorum mating type locus ( MAT) contains a 3.6-kb region that is inverted in every meiotic generation. PLoS One 8 : e56895.[CrossRef]
181. Idnurm A,, Walton FJ,, Floyd A,, Heitman J . 2008. Identification of the sex genes in an early diverged fungus. Nature 451 : 193 196.[PubMed] [CrossRef]
182. Lee SC,, Corradi N,, Byrnes EJ III,, Torres-Martinez S,, Dietrich FS,, Keeling PJ,, Heitman J . 2008. Microsporidia evolved from ancestral sexual fungi. Curr Biol 18 : 1675 1679.[PubMed] [CrossRef]
183. Capella-Gutiérrez S,, Marcet-Houben M,, Gabaldón T . 2012. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10 : 47.[PubMed] [CrossRef]
184. Martin T,, Lu SW,, van Tilbeurgh H,, Ripoll DR,, Dixelius C,, Turgeon BG,, Debuchy R . 2010. Tracing the origin of the fungal α1 domain places its ancestor in the HMG-box superfamily: implication for fungal mating-type evolution. PLoS One 5 : e15199.[CrossRef]
185. Kim HK,, Jo SM,, Kim GY,, Kim DW,, Kim YK,, Yun SH . 2015. A large-scale functional analysis of putative target genes of mating-type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum . PLoS Genet 11 : e1005486.[CrossRef]
186. Grognet P,, Bidard F,, Kuchly C,, Tong LC,, Coppin E,, Benkhali JA,, Couloux A,, Wincker P,, Debuchy R,, Silar P . 2014. Maintaining two mating types: structure of the mating type locus and its role in heterokaryosis in Podospora anserina . Genetics 197 : 421 432.[PubMed] [CrossRef]
187. Ait Benkhali J,, Coppin E,, Brun S,, Peraza-Reyes L,, Martin T,, Dixelius C,, Lazar N,, van Tilbeurgh H,, Debuchy R . 2013. A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina . PLoS Genet 9 : e1003642.[CrossRef]
188. Casselton LA . 2008. Fungal sex genes-searching for the ancestors. BioEssays 30 : 711 714.[PubMed] [CrossRef]
189. Turgeon BG,, Christiansen SK,, Yoder OC, . 1993. Mating type genes in Ascomycetes and their imperfect relatives, p 199 215. In Reynolds DR,, Taylor JW (ed), The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics. C. A. B. International, Wallingford, United Kingdom.[PubMed]
190. Glass NL,, Nelson MA, . 1994. Mating-type genes in mycelial ascomycetes, p 295 306. In Wessels JGH,, Meinhardt F (ed), The Mycota I: Growth, Differentiation and Sexuality. Springer-Verlag, Berlin, Germany.[CrossRef]
191. Dyer PS,, O’Gorman CM . 2011. A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol 14 : 649 654.[PubMed] [CrossRef]
192. Wilson AM,, Wilken PM,, van der Nest MA,, Steenkamp ET,, Wingfield MJ,, Wingfield BD . 2015. Homothallism: an umbrella term for describing diverse sexual behaviours. IMA Fungus 6 : 207 214.[PubMed] [CrossRef]
193. Raju NB,, Perkins DD . 2000. Programmed ascospore death in the homothallic ascomycete Coniochaeta tetraspora . Fungal Genet Biol 30 : 213 221.[CrossRef]
194. Fraser JA,, Heitman J . 2004. Evolution of fungal sex chromosomes. Mol Microbiol 51 : 299 306.[CrossRef]
195. Scazzocchio C . 2006. Aspergillus genomes: secret sex and the secrets of sex. Trends Genet 22 : 521 525.[PubMed] [CrossRef]
196. Yun SH,, Arie T,, Kaneko I,, Yoder OC,, Turgeon BG . 2000. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 31 : 7 20.[PubMed] [CrossRef]
197. Yun SH,, Berbee ML,, Yoder OC,, Turgeon BG . 1999. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc Natl Acad Sci USA 96 : 5592 5597.[PubMed] [CrossRef]
198. Gioti A,, Mushegian AA,, Strandberg R,, Stajich JE,, Johannesson H . 2012. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol Biol Evol 29 : 3215 3226.[CrossRef]