Mushroom Sex: How Do They Do It?

Mushrooms, a type of fungus, have a complex system of sexual reproduction that differs significantly from that of mammals. While mammals typically have two sexes defined by their chromosomal makeup, mushrooms can have multiple sexes or mating types, with some species having as many as 17,000 to 23,000 distinct sexes. This diversity in mushroom sexes is due to the presence of multiple mating loci and the ability to recombine genetic material through direct cellular transfer, resulting in a vast number of sexual variations. The mushroom Schizophyllum commune, for example, has thousands of mating types defined by lipopeptide pheromones and their receptors, showcasing the intricate nature of mushroom sexuality.

Fungi have complex sexual reproduction systems

Fungi encompass a wide variety of organisms, many of which have complex sexual reproduction systems. Fungi are unique in that both their haploid and diploid forms can reproduce. Haploid individuals can reproduce asexually, while diploid forms can produce gametes that combine to create a new generation. This contrasts with multicellular eukaryotes, such as mammals, where adults are typically diploid and produce haploid gametes that unite to form offspring.

Fungi have two primary types of sexual reproduction: homothallism and heterothallism. Homothallism occurs when mating happens within a single individual, meaning each individual is self-fertile. In heterothallism, on the other hand, hyphae from a single individual are self-sterile and require interaction with another compatible individual for mating. Heterothallism is the dominant mating system in Basidiomycota, and about 90% of Agaricomycotina (mushroom-forming fungi) species are heterothallic.

The mating process in fungi is intricate and governed by mating types. Some species within Basidiomycota, such as Schizophyllum commune, possess the most intricate sexual reproduction systems known among fungi. Schizophyllum commune has thousands of mating types, defined by numerous lipopeptide pheromones and their G protein-linked receptors. These pheromones and receptors play a crucial role in mate recognition and sexual development, leading to the formation of fruiting bodies (mushrooms) and meiosis.

Sexual reproduction in fungi typically involves three sequential stages: plasmogamy, karyogamy, and meiosis. Plasmogamy is the fusion of two protoplasts, resulting in the combination of two compatible haploid nuclei within the same cell. Karyogamy is the fusion of these haploid nuclei, forming a diploid nucleus with genetic material from both parents. The resulting cell is called a zygote, which is typically the only diploid cell in the fungus's life cycle.

Fungi exhibit remarkable diversity in their reproductive strategies, with some species reproducing primarily asexually while others rely almost exclusively on sexual reproduction. The mechanism of sexual reproduction in mushrooms, in particular, is of great interest to breeders and growers seeking to cultivate new strains and ensure a consistent supply of edible mushrooms.

Bipolar and tetrapolar mating systems

The mating systems in mushrooms are categorised into two types: bipolar and tetrapolar. Heterothallism is the most common mating system in Basidiomycota and in Agaricomycotina (the mushroom-forming fungi) about 90% of the species are heterothallic.

Bipolar Mating System

A bipolar system is defined by a single genetic locus (MAT) that can have two or multiple alleles. Bipolar organisms mostly have multiple alleles for their A mating locus. The B or a locus has linked genes that code for pheromones and pheromone receptors. The pheromones are short polypeptides with conserved residues and the pheromone receptors belong to the G protein-coupled family of receptors located in the cell membrane. The functions of these genes are to regulate reciprocal nuclear exchange, nuclear migration in both mates and ultimately clamp cell fusion.

Tetrapolar Mating System

A tetrapolar system has two loci, each with two or more specificities. The two unlinked mating-type loci are termed A and B (in Agaricomycotina) or b and a (in Ustilaginomycotina and Pucciniomycotina), both of which can be multiallelic. The A and B mating-type loci encode homeodomain transcription factors and pheromones and pheromone receptors, respectively. The multiallelic tetrapolar mating system is considered to be a novel innovation that could have only evolved once. It is believed that multi-allelic systems favour outcrossing in Basidiomycota.

Transition from Tetrapolar to Bipolar Mating System

The origin of a bipolar mating system from a tetrapolar one has been addressed only in the smut fungi. In a landmark study, Bakkeren and Kronstad (1994) demonstrated that the bipolar mating-type locus of Ustilago hordei was formed from the fusion of the a and b mating-type loci observed in tetrapolar smut fungi into one non-recombining mating-type region with two alleles. Thus, genetic linkage through translocation is the best explanation for the origin of bipolar mating in U. hordei.

Homothallism and heterothallism

Fungi have two main types of sexual reproduction: homothallism and heterothallism. Homothallic species are capable of sexual reproduction from a single organism, i.e., they are self-fertile. They possess male and female reproductive structures on the same thallus, with different cells performing opposite sexual functions. Homothallic meiosis may be maintained in fungi as an adaptation for surviving stressful conditions, promoting homologous meiotic recombinational repair of DNA damages caused by a harsh environment. Examples of homothallic species include several ascomycete fungal species of the genus Cochliobolus, the ascomycete fungus Pneumocystis jirovecii, and the ascomycete fungus Neosartorya fischeri. Homothallism is not very common in Basidiomycota, with only about 10% of species exhibiting this behaviour.

Heterothallic species, on the other hand, have sexes that reside in different individuals. These fungi require two compatible partners to produce sexual spores, with two different individuals contributing nuclei to form a zygote. Heterothallism is the most common mating system in Basidiomycota and Agaricomycotina, with about 90% of species being heterothallic. Examples of heterothallic fungi include Saccharomyces cerevisiae, Aspergillus fumigatus, Aspergillus flavus, Penicillium marneffei, and Neurospora crassa.

Homothallism constitutes a variety of distinct strategies that allow for single individuals to sexually reproduce independently, including primary homothallism, pseudohomothallism, mating type switching, and unisexual reproduction. Primary homothallism is the classic mechanism for achieving self-fertility, where species adhere to the strict genetic requirement of the combined expression of MAT1-1 and MAT1-2 genes in a single genome. In contrast, heterothallism represents a relatively simple and well-understood opposite-mate interaction.

Mating type switching is a form of homothallism where cells of either mating type undergo mitosis to form two identical cells, one of which switches to the opposite mating type, resulting in a mixed colony capable of sexual reproduction. Unidirectional mating type switching occurs in Chromocrea spinulosa, where only cells of one mating type are able to switch. Bidirectional mating type switching, on the other hand, is seen in Saccharomyces cerevisiae, where cells of both mating types can switch. Unisexual reproduction, observed in Cryptococcus neoformans, allows cells of the same mating type to interact and produce sexual spores even in the absence of an opposite mating type partner.

While heterothallism is relatively well understood, homothallism remains understudied due to its genetic complexity and the variety of mechanisms involved. It is believed that homothallic species likely evolved from heterothallic ancestors, and heterothallic species like Neurospora tetrasperma can exhibit pseudo-homothallic behaviour under certain conditions.

The role of pheromones and receptors

The mushroom-producing fungus Schizophyllum commune has thousands of mating types, defined by numerous lipopeptide pheromones and their G-protein-coupled receptors. These pheromones and receptors are encoded by different mating types, which regulate a pathway of sexual development leading to mushroom formation and meiosis. The compatibility of pheromone-receptor pairs is crucial for successful mating. For instance, pheromone Bbp1(1) activates the Bβ2 receptor and four additional Bβ receptors, demonstrating the complexity of their interactions.

The specificity of pheromone-receptor interactions is essential for mate recognition and sexual development in Schizophyllum commune. The presence of multiple mating types and pheromone-receptor combinations maximizes the likelihood of outbreeding while minimizing inbreeding. This complex system of pheromones and receptors allows for a diverse range of potential partners, contributing to the genetic diversity of the species.

In addition, the study of pheromone-receptor interactions in Schizophyllum commune has provided valuable insights into the molecular aspects of pheromone-receptor recognition across a wide range of organisms. By reproducing the interactions in yeast, researchers have gained a better understanding of the underlying mechanisms involved in mate recognition and sexual development.

Furthermore, the evolution of the bipolar mating system in mushrooms, such as Coprinellus disseminatus, involves the loss of mating-type-specific pheromone receptor function. This evolution from a tetrapolar mating system, governed by two unlinked mating loci, to a bipolar system with a single allelic mating locus, has resulted in reduced outcrossing within these species.

Fungi have multiple sexes

While humans have traditionally recognized two genders, male and female, some species of fungi can have thousands of sexes. For instance, Schizophyllum commune, a white, fan-shaped mushroom, has over 23,000 different sexes. This is due to the widespread differentiation in the genetic locations that govern its sexual behavior.

The concept of sexes in fungi is not based on physical differences but rather on genetic variations. Fungi reproduce by bumping into another member of their species and fusing their cells together, exchanging their cell nuclei and genetic information. This simple method of reproduction allows for a vast number of sexes.

The sexes of fungi are determined by two unlinked mating loci, termed A and B, each of which has two alleles: alpha and beta. Each of these alleles can have many different variants or specificities, resulting in thousands of possible unique sexes. For example, the Aα locus has 9 different specificities, Aβ has 32, and Bα and Bβ have 9 specificities each.

Fungi with multiple sexes have a higher chance of finding a compatible mate, as they can mate with any other fungus as long as there is a difference in at least one of the two loci. This promotes genetic diversity and increases the fungi's ability to adapt to various environmental conditions, such as droughts or parasites.

Recent advances in sequencing technologies have enabled researchers to better understand the genetic diversity underlying the mating systems of fungi, leading to discoveries of various fungal species with a high number of sexes.

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