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Fungal Sex: the Basidiomycota Marco Coelho, Guus Bakkeren, Sheng Sun, Michael Hood, Tatiana Giraud

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Fungal Sex: the Basidiomycota Marco Coelho, Guus Bakkeren, Sheng Sun, Michael Hood, Tatiana Giraud Fungal Sex: The Basidiomycota Marco Coelho, Guus Bakkeren, Sheng Sun, Michael Hood, Tatiana Giraud To cite this version: Marco Coelho, Guus Bakkeren, Sheng Sun, Michael Hood, Tatiana Giraud. Fungal Sex: The Ba- sidiomycota. Microbiology Spectrum, American Society for Microbiology, 2017, 5 (3), pp.147-175. 10.1128/microbiolspec.FUNK-0046-2016. hal-02328823 HAL Id: hal-02328823 https://hal.archives-ouvertes.fr/hal-02328823 Submitted on 10 Mar 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. The Fungal Kingdom Edited by J. Heitman, B. J. Howlett, P. W. Crous, E. H. Stukenbrock, T. Y. James, and N. A. R. Gow © 2018 American Society for Microbiology, Washington, DC doi:10.1128/microbiolspec.FUNK-0046-2016 Fungal Sex: The Basidiomycota Marco A. Coelho,1 Guus Bakkeren,2 Sheng Sun,3 4 5 7 Michael E. Hood, and Tatiana Giraud BREEDING SYSTEMS AND LIFESTYLES pendently evolving lineages are strongly within the IN THE BASIDIOMYCOTA Basidiomycota (Fig. 2) (3). The subphylum Agarico- In the phylum Basidiomycota, a wide variety of life- mycotina contains most of the described species (ca. styles are represented. These range from well-known 21,000), including many mushrooms as saprophytes and conspicuous wood-decaying mushrooms, plant or mycorrhizal symbionts of plants, the jelly fungi, and growth-promoting and mutualistic mycorrhizae, and a large diversity of yeasts, some of which are important crop-destroying smut and rust fungi, to yeast-like hu- pathogens of humans (viz., Cryptococcus neoformans) man pathogens. Lifestyle differences have consequences (4, 5). The subphylum Ustilaginomycotina comprises for the mating and breeding systems of these fungi (see more than 1,700 species, and while many species are “Glossary,” below, for definitions of specialist terms pathogens of graminaceous plants (such as the maize used in this article), which are reflected in the genetic smut Ustilago maydis), others are commonly associated evolution of mating-type determination. For over a with human and animal infections and are known from century fungi have been recognized as having diverse their asexual (anamorphic) states only (viz., Malassezia breeding systems, from homothallism (i.e., universal spp.) (4, 6, 7). The subphylum Pucciniomycotina is a compatibility among gametes, including among clone- sister group of the clade containing Ustilaginomyco- mates) to heterothallism (i.e., mating among haploid tina and Agaricomycotina and consists of more than gametes carrying different mating-type alleles). The 8,400 described species (8). Besides the array of sapro- study of breeding systems, for example, led to the dis- bic yeast species usually recovered from soils, aquatic covery of the astounding variability in mating-type habitats, or the phylloplane (e.g., Rhodotorula spp. and alleles among mushrooms, with thousands of different Sporobolomyces spp.) (9), most of the Pucciniomyco- mating types in some species (1), and to the realization tina species are plant parasites, such as the obligate that in many fungal pathogens the process of sexual pathogenic rust fungi (e.g., Puccinia spp.) or anther- reproduction is closely linked to infection and patho- smut fungi (Microbotryum spp.). Through the diversifi- genicity (2) (Fig. 1). The importance of basidiomycete cation of mating and dispersal stages, this huge variety fungi and their great research tractability, from ecology of fungal lifestyles is highly integrated with equally di- to genomics, have brought major insights into the diver- verse sexual cycles and breeding systems, a theme that sification of genetic mechanisms used to achieve sexual has long been the subject of study by influential mycol- reproduction. ogists (1, 10–13). Diversity and Phylogenetic Relationships: Sexual Development and Determination Phylum Basidiomycota of Cell Type Identity From a phylogenetic perspective, the phylum Basidio- Most fungi are able to undergo both asexual and sexual mycota is the sister group to the phylum Ascomycota, reproduction and have evolved tightly controlled mech- forming together the subkingdom Dikarya. Three inde- anisms to regulate the process of mating, with respect 1UCIBIO-REQUIMTE, Departamento de Cieˆncias da Vida, Faculdade de Cieˆncias e Tecnologia, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal; 2Agriculture and Agri-Food Canada, Summerland Research and Development Centre, Summerland, BC, V0H 1Z0, Canada; 3Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4Department of Biology, Amherst College, Amherst, MA 01002; 5Ecologie Syste´matique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Universite´ Paris-Saclay, 91400, Orsay, France. 147 148 LIFE OF FUNGI 7. FUNGAL SEX:THE BASIDIOMYCOTA 149 to timing, and gamete dispersal, recognition, and fusion. (MAT) locus (see reference 197). In that case, only two In basidiomycetes, the sexual cycle typically involves mating types segregate in meiosis, defining what is fusion of genetically distinct homokaryotic hyphae or termed a bipolar system. By contrast, basidiomycetes haploid yeast cells to produce a dikaryon, in which the have evolved a breeding system that relies on two ge- two haploid parental nuclei are replicated in a coordi- netic MAT loci. One locus encodes tightly linked phero- nated fashion without fusion during hyphal elongation, mones and pheromone receptors (hereafter referred to usually involving the formation of clamp connections as the P/R locus), and the other encodes homeodomain- (i.e., a hook-like structure formed by hyphal cells to en- type transcription factors (hereafter, HD locus), de- sure proper distribution of the two genetically distinct termining viability following syngamy. For successful nuclei during mitotic cell divisions; see below) (14). Nu- mating and completion of the sexual cycle, haploid clear fusion (karyogamy) then takes place in the basidia cells that conjugate must differ at both MAT loci (18, or in other specialized structures (e.g., teliospores), after 19). When the two MAT loci are unlinked, four mating which the diploid nucleus undergoes meiosis to generate types can be generated by meiosis among the haploid haploid basidiospores (meiospores) and complete the progeny, defining this as a tetrapolar breeding system. life cycle (see Fig. 1 for representative life cycles). Other basidiomycetes have instead a bipolar system con- Despite the wide variation of sexual cycles in nature, trolled by a single MAT locus, either because the P/R one common underlying feature shared by most fungi and HD loci are linked or because one has lost its func- is the lack of genetically determined anisogamy: many tion in mating-type determinism. In mushroom-forming fungi are isogamous (i.e., where all gametes have the species (Agaricomycetes), there has been a generalized same sizes), and even in anisogamous species, all hap- diversification of alleles at both MAT loci, in some cases loid genotypes produce both types of gamete sizes. This yielding species with hundreds or thousands of possi- means that there are not individuals of different sexes ble mating types (1, 20–22). Data compiled from early in fungi (15). Furthermore, many fungi are heterothal- studies indicate that as many as 65% of the species in lic, meaning that syngamy can only occur between the Agaricomycotina are tetrapolar (13, 23), whereas gametes of different genetically determined mating types classical mating studies indicate a predominance of (15–17). bipolar systems in the majority of the Ustilaginomyco- In members of the sister phylum Ascomycota, mating- tina (24) and the Pucciniomycotina (25). In the follow- type identity is governed at a single genetic mating type ing sections we summarize current knowledge of the Figure 1 General life cycles of dimorphic and mushroom-forming basidiomycetes. Three basidiomycetes are pictured where sexual reproduction and a dimorphic switch between a yeast cell and a hyphal form are crucial to infection of plant (A, B) or animal (C) hosts. The haploid yeast forms of the maize smut Ustilago maydis (A) and the anther smut Micro- botryum spp. (B) are nonpathogenic and can undergo asexual mitotic vegetative growth. In Microbotryum, the yeast stage is, however, short-lived because mating occurs mostly be- tween cells within the same tetrad. Upon mating with a compatible partner, both fungi switch to an enduring infection hyphal form (dikaryon; n + n) that can invade the host plant. Proliferation and differentiation of U. maydis (A) in the plant culminates with the produc- tion of masses of wind-dispersing diploid spores (teliospores; 2n) in large tumor-like tissues, whereas in Microbotryum (B), teliospores are formed in the anthers of infected flowers and transmitted by pollinators onto healthy plants. In the case of Cryptococcus neoformans (C), the single-celled yeast form may be free-living or mycoparasitic. A similar dimorphic switch occurs upon mating of yeast cells of opposite mating type (α or α), ultimately resulting in the infectious propagules (basidiospores)
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