21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 7: From the haploid to the functional diploid; homokaryons, heterokaryons, dikaryons and compatibility
2. Chapter 8: Sexual reproduction: the basis of diversity and taxonomy
   1. The process of sexual reproduction
   2. Mating in budding yeast
   3. Mating type switching in budding yeast
   4. Mating types of Neurospora
   5. Mating types in Basidiomycota
   6. Biology of mating type factors
   7. Chapter 8 References and further reading
   8. Buy a PDF of Chapter 8
3. Chapter 9: Continuing the diversity theme: cell and tissue differentiation

8.6 Biology of mating type factors

Mating type factors are transcription regulators, together with pheromones and their receptors that create the circumstances promoting meiosis. Surprisingly, they're not universal. Many fungi get by perfectly well without mating types. In Podospora, the progress of meiosis and sporulation does not require heterozygous mating type factors, the organism is homothallic, and homothallism occurs even in higher mushroom fungi; the Paddy Straw mushroom Volvariella volvacea is homothallic. Even in Coprinopsis cinerea and Schizophyllum commune, apparently normal fruiting bodies can be formed by haploid cultures, and fruit body formation can usually be separated from other parts of the sexual pathway, by mutation, in all species that have a well-developed mating type system.

Therefore, the significance of mating type factors in regulating events beyond the initial mating reaction is difficult to judge; indeed, given the success of anamorphic fungi, understanding the selective advantage of sexual reproduction itself needs careful argument (Anderson & Kohn, 1998; see chapter 9 in Moore, 2001; see chapter 2 in Moore & Novak Frazer, 2002; Pringle & Taylor, 2002; Heitman, 2015).

Mating type factors are usually interpreted as promoting outbreeding by preventing breeding between closely related progeny. With only two idiomorphs, the likelihood that two individuals will be able to mate (which is the outbreeding potential) is 50%. But if there were n mating type idiomorphs the outbreeding potential would be [1/n × (n-1)] × 100%; so the greater the number of mating type idiomorphs, the greater the outbreeding potential.

In the case of the Basidiomycota with a bifactorial incompatibility system with two unlinked mating type factors (designated A and B), a compatible interaction is one between two mycelia with different idiomorphs, but now both A and B mating type factors must differ. As a result, the diploid nucleus that is formed will be heterozygous at the two mating type loci and meiosis will generate progeny spores of four different mating types (which is why tetrapolar heterothallism is the alternative name of this system).

Coprinopsis cinerea and Schizophyllum commune are the classic examples of this mating type system. In both of these the wild population contains many different A and B idiomorphs, and the outbreeding potential approaches 100%. The inbreeding potential of bifactorial incompatibility (the likelihood of being able to mate with a sibling) is 25% (because there are four different mating types among the progeny of a single meiosis) whereas inbreeding and outbreeding potentials are both 50% in unifactorial incompatibility where there are only two mating types among the progeny. So a bifactorial system tends to favour outbreeding. About 90% of higher fungi are heterothallic, and 40% of these are bipolar and 60% tetrapolar.

Implicit in the calculations of the two paragraphs above is the fact that fungi are eukaryotes and their basic genetics follows the pattern seen in other higher organisms. So unlinked genes undergo Mendelian segregations, just like the genes of Mendel’s garden peas, and linked genes show recombination in frequencies characteristic of their distance apart, just like linked genes in fruit flies. What differences exist arise from peculiarities in the biology of the fungal lifestyle, such as:

• most fungi are haploid, which makes analysis of gene segregations in crosses more direct and provides a tool for the experimenter to use selection methods to find very mutations, or rare recombinants;
• sibling meiotic products tend to be grouped together (ascospores in asci, basidiospores on basidia), which gives the geneticist an opportunity to bring centromere segregation into the analysis, a tool that is only very rarely available in other eukaryotes.

We do not intend to discuss the basic genetics of fungi any further here and urge you to read the book Essential Fungal Genetics by Moore & Novak Frazer (2002), especially their Chapter 5 [CLICK HERE to view directly]; and Dyer et al., 2017).

Tetrapolar mating systems not only promote outbreeding but also lead to inbreeding depression. These differences in the frequencies of outbreeding and inbreeding are thought to provide the evolutionary pressure for transitions between bipolar and tetrapolar mating systems. Phylogenetic reconstructions across the fungal kingdom support the conclusion that bipolar mating is an ancestral state and the tetrapolar configuration is a derived state. All species with known mating type systems in the zygomycetes and ascomycetes are bipolar. This is in marked contrast to the basidiomycetes in which most species have a tetrapolar mating system. Though there are examples of species with bipolar mating type within the Basidiomycota, so far, no species with the tetrapolar mating system have been found outside of the Basidiomycota and this leads to the conclusion that the tetrapolar system is a derived state, possibly with a single origin at the base of the Basidiomycota.

Presumably, an ancestral system with just one MAT locus encoding homeodomain factors evolved into a system with a second sex determinant on another chromosome encoding pheromones and pheromone receptors. We must then make the further deduction that the bipolar mating systems of pathogenic basidiomycete species have been derived from the tetrapolar system and that this transition from tetrapolar to bipolar has occurred several times independently during evolution of the Basidiomycota (Heitman, 2015).

Updated July, 2019