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Chapter 9 : Sex and the Imperfect Fungi

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Abstract:

Sexual reproduction is a ubiquitous feature of the eukaryotic kingdom with the many benefits of sex in generating genetic diversity as substrates for evolutionary selection being well known. When two different partners come together, there is the generation of genetic variation in the offspring, through the processes of crossover and recombination during meiosis, enabling response of future generations to environmental selection pressures ( ). Sexual reproduction also allows the repair of random epigenetic or conventional genetic damage by recombination with homologous chromosomes and can mask lethal mutations ( ). In addition, sexual recombination alleviates clonal interference and prevents deleterious mutations hitchhiking to fixation ( ). Indeed, there are so many benefits to sexual reproduction that exceptions that are purely asexual have been termed “evolutionary scandals” ( ). As a result, supposed ancient asexual species such as the bdelloid rotifers (an exclusively female class of over 460 rotifer species thought to date back several million years) and darwinulid ostracods (a family of around 30 crustacean species thought to have been exclusively female and asexual for over 200 million years, but for which very rare living males have recently been described) have gained notoriety ( ). It therefore comes as a great surprise that, until recently, approximately 20% of all fungal species were considered to reproduce only by asexual means, with no recognized sexual cycle, based on knowledge of described fungal species ( ). Indeed, in some phylogenetic groupings such as the Ascomycotina, up to 40% of taxa surveyed were deemed to be asexual ( ). This is despite the fact that sexual reproduction in fungi can have additional benefits such as the production of fruit bodies and sexual spores that are resistant to adverse environmental conditions, thereby promoting survival of sexual offspring; it can provide a transient diploid arena for selection of genes; and sex can favorably impact genome evolution ( ). Asexual species are also proposed to be short-lived evolutionary “dead ends” subject to rapid extinction ( ). Fungal species lacking a known sexual cycle have been referred to as “imperfect” or “mitosporic” fungi and have been grouped into the “Fungi Imperfecti” or “Deuteromycota,” although phylogenetic analysis has shown that these are artificial groupings not based on taxonomic relationship ( ). The terms “asexual” and “imperfect” are used synonymously in this review.

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-0043-2017
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Figures

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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 ( ). For , the gene designation is as previously published by Paoletti et al. ( ). 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 ).

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-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).

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-0043-2017
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Image of Figure 3
Figure 3

Target genes of the locus encoded transcription factors from , deduced from functional genomics experiments ( ). 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 ).

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-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 ).

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-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).

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-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

Citation: Dyer P, Kück U. 2017. Sex and the Imperfect Fungi, p 193-214. 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-0043-2017

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