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Chapter 6 : Fungal Sex: The

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Abstract:

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
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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
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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
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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
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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
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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
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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
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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
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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
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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
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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
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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
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