Sex and the Imperfect Fungi

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 Candida, Aspergillus, Penicillium, and Trichoderma 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.

FIGURE 1

Comparison of MAT loci from homo- and heterothallic members of the Eurotiales. Blue arrows indicate a MATα-domain gene, red arrows indicate a MAT high-mobility group gene, black bars indicate intronic sequences, gray bars homologous sequences (48, 49, 51, 173). For A. nidulans, the gene designation is as previously published by Paoletti et al. (49). Note that, whereas isolates of heterothallic species contain only one MAT idiomorph (either MAT1-1 or MAT1-2), isolates of homothallic species contain both types of MAT gene in the same genome (i.e., both MAT1-1 and MAT1-2).

FIGURE 2

Occurrence of both MAT idiomorphs in wild-type isolates from Penicillium chrysogenum. Blue and red dots represent strains with the MAT1-1 or MAT1-2 locus, respectively (C. M. O’Gorman and U. Kück, unpublished data).

FIGURE 3

Target genes of the MAT1-1-1 locus encoded transcription factors from Penicillium chrysogenum, 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).

FIGURE 4

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

FIGURE 5

Sclerotia formation (arrowed large gray-brown spheres) in Aspergillus niger, 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 MAT1-1-1 genotype (H. Darbyshir, G. Ashton, and P. S. Dyer, unpublished data).