6 Mating Type in Basidiomycetes: Unipolar, Bipolar, and Tetrapolar Patterns of Sexuality

Kües, Ursula; James, Timothy Y.; Heitman, Joseph

doi:10.1007/978-3-642-19974-5_6

Cited by 92 publications

(185 citation statements)

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“…In bipolar species, P/R and HD genes are genetically linked at a single MAT locus and therefore only two mating types are generated after meiosis (referred to as "A1" and "A2" or "a" and "a"). In contrast, in tetrapolar species, P/R and HD genes are located at two physically unlinked genomic regions that segregate independently during meiosis to generate up to four different mating types (Kües et al 2011;Heitman et al 2013;Nieuwenhuis et al 2013). Despite these fundamental differences, individuals that are brought together must carry different alleles at both MAT loci for sexual reproduction to occur (reviewed in Kües et al 2011;Nieuwenhuis et al 2013).…”

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“…Interestingly, most of the known tetrapolar yeast species exhibit a biallelic P/R locus and a multiallelic HD locus (viz. Ustilago maydis, Kwoniella heveanensis, Kwoniella mangrovensis, Cryptococcus amylolentus) (Bölker et al 1992;Kämper et al 1995;Metin et al 2010;Findley et al 2012;Guerreiro et al 2013), a configuration originally designated as "modified tetrapolar" by Robert J. Bandoni to denote that outcrossing in such a system cannot exceed 50% (Bandoni 1963;Kües et al 2011). Indeed, only by evolving multiple alleles at both MAT loci can a tetrapolar system maximize the outcrossing efficiency to .50%, as observed in mushroomforming species (viz.…”

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“…This work uncovered a mating system that appeared to deviate from the classical bipolar and tetrapolar mating paradigms based on two main observations: first, a worldwide collection of natural isolates of S. salmonicolor revealed that only two alleles (A1 and A2) exist at the P/R locus, each of which appears to be linked to multiple (yet specific) alleles at the HD locus; and second, the progeny of a cross between compatible strains indicate that recombination/ assortment of P/R and HD loci may occur, albeit at a low frequency (Coelho et al 2010). Therefore, to denote the distinction between the strictly bipolar mating behavior of S. salmonicolor strains isolated from nature and the apparent tetrapolar pattern of inheritance of mating-type genes in laboratory crosses, this mating system was named "pseudobipolar" (Coelho et al 2010).Even though the tetrapolar system appears to be exclusive of the phylum Basidiomycota (Kües et al 2011;Heitman et al 2013;Nieuwenhuis et al 2013), it is currently equivocal if the last common ancestor of the basidiomycetes had a tetrapolar or bipolar mating system. Reconstructing the evolutionary path leading to the present mating systems of basidiomycetes requires obtaining information on this trait for several extant bipolar and tetrapolar members of the three major lineages.…”

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“…The ancestral state in fungi is likely to be bipolar given the presence of this system in both the Dikarya and Mucoromycotina (Idnurm et al 2008;Heitman et al 2013;Nieuwenhuis et al 2013). A bipolar-to-tetrapolar transition is therefore assumed to have occurred in the Basidiomycota, and genomic footprints suggest that bipolar species within this lineage have evolved secondarily, either by linkage of the two MAT loci or due to the loss of the P/R locus as an incompatibility determinant (Kües et al 2011;Heitman et al 2013;James et al 2013;Nieuwenhuis et al 2013). However, owing to the occurrence of a myriad of bipolar species within the basidiomycetes, and the paucity of molecular data regarding tetrapolar mating systems in the more basally derived Pucciniomycotina lineage, it has been debatable whether or not tetrapolarity had a single point of origin.…”

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“…These genes encode premating lipopeptide pheromones and their cognate receptors (P/R), which mediate recognition of mating partners and cell fusion, and homeodomain transcription factors (HD1 and HD2) that form heterodimers that regulate postmating behavior (Kües et al 2011;Nieuwenhuis et al 2013). Over the years, it has been shown that basidiomycetes may occur in two different mating configurations: bipolar and tetrapolar.…”

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Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

et al. 2015

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In most fungi, sexual reproduction is bipolar; that is, two alternate sets of genes at a single mating-type (MAT) locus determine two mating types. However, in the Basidiomycota, a unique (tetrapolar) reproductive system emerged in which sexual identity is governed by two unlinked MAT loci, each of which controls independent mechanisms of self/nonself recognition. Tetrapolar-to-bipolar transitions have occurred on multiple occasions in the Basidiomycota, resulting, for example, from linkage of the two MAT loci into a single inheritable unit. Nevertheless, owing to the scarcity of molecular data regarding tetrapolar systems in the earliest-branching lineage of the Basidiomycota (subphylum Pucciniomycotina), it is presently unclear if the last common ancestor was tetrapolar or bipolar. Here, we address this question, by investigating the mating system of the Pucciniomycotina yeast Leucosporidium scottii. Using whole-genome sequencing and chromoblot analysis, we discovered that sexual reproduction is governed by two physically unlinked gene clusters: a multiallelic homeodomain (HD) locus and a pheromone/receptor (P/R) locus that is biallelic, thereby dismissing the existence of a third P/R allele as proposed earlier. Allele distribution of both MAT genes in natural populations showed that the two loci were in strong linkage disequilibrium, but independent assortment of MAT alleles was observed in the meiotic progeny of a test cross. The sexual cycle produces fertile progeny with similar proportions of the four mating types, but approximately 2/3 of the progeny was found to be nonhaploid. Our study adds to others in reinforcing tetrapolarity as the ancestral state of all basidiomycetes.KEYWORDS sexual reproduction; mating type; mating-type determination; fungi; Basidiomycota S EXUAL reproduction has a pivotal role in the biology of many eukaryotes and is likely a defining evolutionary innovation of this lineage (Dacks and Roger 1999;Goodenough and Heitman 2014). In addition to promoting genetic variation, required for adaptation to fluctuating environments and longterm survival, sexual reproduction in many fungal species, in particular, has a central role in pathogenic development (Bakkeren et al. 2008;Nadal et al. 2008;Heitman 2010;Heitman et al. 2014). It is thus not surprising that recent advances in genome sequencing have revealed that most fungal species have retained the machinery for sexual reproduction and meiosis (Halary et al. 2011;Dyer and O'Gorman 2012;Gioti et al. 2013;Heitman et al. 2014). However, this resilience to keep sexual competence intact comes with an extremely dynamic evolution of sexual behaviors and mating type-determining mechanisms, which may influence important evolutionary and ecological processes, such as adaptation and speciation (Billiard et al. 2011;Heitman et al. 2013;Nieuwenhuis et al. 2013).In the phylum Basidiomycota, sexual reproduction is often dictated by two independent sets of mating-type (MAT)-specific genes that control different stages of the sexual cycle. These...

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Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

et al. 2015

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The evolution of mating‐type switching for reproductive assurance

Nieuwenhuis

Immler

2016

BioEssays

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Alternative ways to ensure mate compatibility, such as hermaphroditism and the breakdown of self-incompatibility, evolved repeatedly when finding a mating partner is difficult. In a variety of microorganisms where compatibility is determined by mating-types, a highly regulated form of universal compatibility system called mating-type switching has evolved several times. This sophisticated system allows for the genetic adjustment of the mating type during asexual growth, and it most likely evolved for reproductive assurance of immotile species under low densities. In this review, we compare the switching strategy to other universal compatibility systems such as "unisexual mating" and homothallism. We identify the costs of switching, including genome instability, and mechanistic costs, as well as the benefits, mainly the maintenance of important mating-type functions. Given the potential benefits of mating-type switching, we speculate that switching is likely to have evolved many times independently, and may be more common in groups where genetic mating types regulate mate compatibility than assumed so far.

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Genome Evolution of Asexual Organisms and the Paradox of Sex in Eukaryotes

Hörandl

Bast

Brandt

et al. 2020

Evolutionary Biology—A Transdisciplinary Approach

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The predominance of sex in eukaryotes is still enigmatic. Sex, a composed process of meiosis and mixis cycles, confers high costs but the selective advantages remain unclear. In this review, we focus on potentially detrimental effects of asexuality on genome evolution. Theory predicts that asexual lineages should suffer from lack of meiotic DNA repair, accumulation of deleterious mutations, proliferation

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6 Mating Type in Basidiomycetes: Unipolar, Bipolar, and Tetrapolar Patterns of Sexuality

Cited by 92 publications

References 341 publications

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

The evolution of mating‐type switching for reproductive assurance

Genome Evolution of Asexual Organisms and the Paradox of Sex in Eukaryotes

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