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Sex and the Imperfect Fungi

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  • Authors: Paul S. Dyer1, Ulrich Kück2
  • Editors: Joseph Heitman3, Neil A. R. Gow4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: School of Life Sciences, University Park, University of Nottingham, Nottingham, NG7 2RD, United Kingdom; 2: Lehrstuhl für Allgemeine und Molekulare Botanik, Ruhr-University Bochum, 44780 Bochum, Germany; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
  • Received 08 February 2017 Accepted 22 February 2017 Published 09 June 2017
  • Paul S. Dyer, paul.dyer@nottingham.ac.uk
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  • Abstract:

    Approximately 20% of species in the fungal kingdom are only known to reproduce by asexual means despite the many supposed advantages of sexual reproduction. However, in recent years, sexual cycles have been induced in a series of emblematic “asexual” species. We describe how these discoveries were made, building on observations of evidence for sexual potential or “cryptic sexuality” from population genetic analyses; the presence, distribution, and functionality of mating-type genes; genome analyses revealing the presence of genes linked to sexuality; the functionality of sex-related genes; and formation of sex-related developmental structures. We then describe specific studies that led to the discovery of mating and sex in certain , , , and species and discuss the implications of sex including the beneficial exploitation of the sexual cycle. We next consider whether there might be any truly asexual fungal species. We suggest that, although rare, imperfect fungi may genuinely be present in nature and that certain human activities, combined with the genetic flexibility that is a hallmark of the fungal kingdom, might favor the evolution of asexuality under certain conditions. Finally, we argue that fungal species should not be thought of as simply asexual or sexual, but rather as being composed of isolates on a continuum of sexual fertility.

  • Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi. Microbiol Spectrum 5(3):FUNK-0043-2017. doi:10.1128/microbiolspec.FUNK-0043-2017.

Key Concept Ranking

Restriction Fragment Length Polymorphism
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0.41389108

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0043-2017
2017-06-09
2017-11-22

Abstract:

Approximately 20% of species in the fungal kingdom are only known to reproduce by asexual means despite the many supposed advantages of sexual reproduction. However, in recent years, sexual cycles have been induced in a series of emblematic “asexual” species. We describe how these discoveries were made, building on observations of evidence for sexual potential or “cryptic sexuality” from population genetic analyses; the presence, distribution, and functionality of mating-type genes; genome analyses revealing the presence of genes linked to sexuality; the functionality of sex-related genes; and formation of sex-related developmental structures. We then describe specific studies that led to the discovery of mating and sex in certain , , , and species and discuss the implications of sex including the beneficial exploitation of the sexual cycle. We next consider whether there might be any truly asexual fungal species. We suggest that, although rare, imperfect fungi may genuinely be present in nature and that certain human activities, combined with the genetic flexibility that is a hallmark of the fungal kingdom, might favor the evolution of asexuality under certain conditions. Finally, we argue that fungal species should not be thought of as simply asexual or sexual, but rather as being composed of isolates on a continuum of sexual fertility.

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Figures

Image of FIGURE 1
FIGURE 1

Comparison of loci from homo- and heterothallic members of the Eurotiales. Blue arrows indicate a α-domain gene, red arrows indicate a high-mobility group gene, black bars indicate intronic sequences, gray bars homologous sequences ( 48 , 49 , 51 , 173 ). For , the gene designation is as previously published by Paoletti et al. ( 49 ). Note that, whereas isolates of heterothallic species contain only one idiomorph (either or ), isolates of homothallic species contain both types of gene in the same genome (i.e., both and ).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
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Image of FIGURE 2
FIGURE 2

Occurrence of both idiomorphs in wild-type isolates from . Blue and red dots represent strains with the or locus, respectively (C. M. O’Gorman and U. Kück, unpublished data).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
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FIGURE 3

Target genes of the locus encoded transcription factors from , deduced from functional genomics experiments ( 58 , 61 ). In particular, ChIP-seq analysis has shown that MAT1-1-1 regulates gene expression far beyond their described function as regulator of sexual development (modified from reference 174 ).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
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FIGURE 4

Summary of the regulatory functions of locus encoded transcription factors MAT1-1-1 and MAT1-2-1 in (modified according to reference 175 ).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
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FIGURE 5

Sclerotia formation (arrowed large gray-brown spheres) in , an indication of the potential for sex in this biotechnologically important species? Scale bar indicates 500 μm. Note that this species is predominantly of the genotype (H. Darbyshir, G. Ashton, and P. S. Dyer, unpublished data).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017
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Tables

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TABLE 1

Evidence for mating-type loci, their distribution, functional characterization, and induction of a sexual cycle in representative euascomycete species that have been presumed to be asexual

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0043-2017

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