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Fungal Sex: The

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  • Authors: Richard J. Bennett1, B. Gillian Turgeon2
  • Editor: Joseph Heitman3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Molecular Microbiology and Immunology, Brown University, Providence, RI 02912; 2: Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710
  • Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
  • Received 16 March 2016 Accepted 09 May 2016 Published 21 October 2016
  • Richard J. Bennett, Richard_Bennett@brown.edu, and B. Gillian Turgeon, bgt1@cornell.edu
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  • Abstract:

    This article provides an overview of sexual reproduction in the ascomycetes, a phylum of fungi that is named after the specialized sacs or “asci” that hold the sexual spores. They have therefore also been referred to as the Sac Fungi due to these characteristic structures that typically contain four to eight ascospores. Ascomycetes are morphologically diverse and include single-celled yeasts, filamentous fungi, and more complex cup fungi. The sexual cycles of many species, including those of the model yeasts and and the filamentous saprobes , , and , have been examined in depth. In addition, sexual or parasexual cycles have been uncovered in important human pathogens such as and , as well as in plant pathogens such as and . We summarize what is known about sexual fecundity in ascomycetes, examine how structural changes at the mating-type locus dictate sexual behavior, and discuss recent studies that reveal that pheromone signaling pathways can be repurposed to serve cellular roles unrelated to sex.

  • Citation: Bennett R, Turgeon B. 2016. Fungal Sex: The . Microbiol Spectrum 4(5):FUNK-0005-2016. doi:10.1128/microbiolspec.FUNK-0005-2016.

Key Concept Ranking

Single Nucleotide Polymorphism
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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0005-2016
2016-10-21
2017-09-23

Abstract:

This article provides an overview of sexual reproduction in the ascomycetes, a phylum of fungi that is named after the specialized sacs or “asci” that hold the sexual spores. They have therefore also been referred to as the Sac Fungi due to these characteristic structures that typically contain four to eight ascospores. Ascomycetes are morphologically diverse and include single-celled yeasts, filamentous fungi, and more complex cup fungi. The sexual cycles of many species, including those of the model yeasts and and the filamentous saprobes , , and , have been examined in depth. In addition, sexual or parasexual cycles have been uncovered in important human pathogens such as and , as well as in plant pathogens such as and . We summarize what is known about sexual fecundity in ascomycetes, examine how structural changes at the mating-type locus dictate sexual behavior, and discuss recent studies that reveal that pheromone signaling pathways can be repurposed to serve cellular roles unrelated to sex.

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Figures

Image of FIGURE 1
FIGURE 1

Phylogenetic relationships of major groups of fungi. Synthesis from references 280 282 . 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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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 a 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 a 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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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 111 .

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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).

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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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.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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Image of FIGURE 11
FIGURE 11

Phylogenetic relationships among members of the HMG-box superfamily. Adapted from Fig. 3 of reference 184 and Fig. 2 of reference 187 . 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, .

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0005-2016
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