Mushroom Mysteries: Chromosomes In Fungi

Mushrooms are the reproductive structures of fungi, and they play a key role in the sexual reproduction of these organisms. Fungi have two main types of sexual reproduction: homothallism, where mating occurs within a single individual, and heterothallism, where hyphae from a single individual need to interact with another compatible individual to mate. The process of sexual reproduction in mushrooms involves the fusion of haploid nuclei to form diploid nuclei with a full complement of chromosomes. This occurs within specialized sexual cells called basidia, and the resulting spores produced are dispersed to start the life cycle anew. While most mushroom species are thought to have cells that are dikaryotic, containing two genetically distinct haploid nuclei, recent studies have found that some species, such as Armillaria, have somatic cells that contain a single diploid nucleus. Furthermore, the mating process in mushrooms is influenced by mating types and loci, which determine compatibility. The study of mushroom chromosomes provides insights into the evolution of multicellular fungi and their complex mating systems.

Chromosomes in cultivated mushrooms

The mushroom Coprinopsis cinerea, previously known as Coprinus cinereus, has been a key species in advancing our understanding of fungal biology, evolution, and biomedical implications. Its relatively short life cycle, defined media requirements, and amenability to manipulation at all developmental stages make it an ideal experimental model for studying multicellular development in fungi. The 37-megabase genome of C. cinerea has been sequenced and assembled into 13 chromosomes, revealing insights into meiotic chromosome behaviour and gene distribution.

Analyses of the C. cinerea genome have revealed that meiotic recombination rates vary significantly along the chromosomes. Regions with low meiotic recombination rates tend to be enriched with genes related to fundamental structures and processes, such as nitrogen metabolism, the cytoskeleton, and metabolic regulation. These regions also exhibit a notable absence of transposable elements.

Furthermore, the distribution of gene families along the chromosomes has been observed. Single-copy genes with identifiable orthologs in other basidiomycetes are predominantly found in low-recombination regions, while paralogous multicopy genes are prevalent in highly recombining regions. This includes a unique family of protein kinases (FunK1) specific to multicellular fungi. These insights contribute to our understanding of the evolution and complexity of multicellular fungi.

Wild mushroom chromosomes

While there is a wealth of information on the chromosomes of cultivated mushrooms, very little work has been done on the cytology of wild mushrooms. One source mentions the wild mushroom Agaricus campestris Fr. var. tetrasporus, which has not been successfully crossed with its cultivated form.

The mushroom Coprinopsis cinerea (formerly known as Coprinus cinereus) is a classic experimental model for studying the evolution of multicellular fungi. Its 37-megabase genome has been sequenced and assembled into 13 chromosomes. Analyses of its chromosomes have revealed insights into the evolution of multicellular fungi, including blocks of shared ancestral gene order, the consequences of whole-genome duplication, and the location of large gene families near chromosome ends.

Studies on C. cinerea have also provided important insights into meiotic chromosome behavior. Meiosis occurs with a high degree of synchrony, and meiotic mutants have been obtained and analyzed using cytological and molecular tools. Serial sectioning and three-dimensional reconstruction have been used to describe the karyotype, synaptic initiation sites, and the dynamics of recombination nodule assembly and chiasmata.

Additionally, the chromosomal regions that are unusually refractory to rearrangement in mushrooms have been identified. These regions are found primarily on the five largest chromosomes and are enriched in genes related to basic structures and processes, such as nitrogen metabolism, the cytoskeleton, and metabolic regulation. They also contain a higher number of expected transcription factors and lack transposable elements.

Haploid vs. diploid nuclei

Mushrooms, like other fungi, have alternating life cycles where both haploid and diploid forms occur naturally in nature, called alternation of generations. The fruiting structure of a mushroom produces spores, which are capable of forming free-living haploid individuals through continued cell division. These spores can also fuse to form sexual diploid individuals.

Haploid cells contain one full set of chromosomes and are usually germ cells. They are formed through meiosis, a process that reduces the chromosome number. Haploid cells are genetically diverse, and when a male and female haploid cell fuse during fertilization, they form a diploid cell.

Diploid cells, on the other hand, contain two full sets of chromosomes. They are present in most animals and many plants, and all somatic (body) cells in these organisms are diploid. Diploid cells are created via mitosis, a process that conserves the chromosomal number, resulting in daughter cells with equal chromosome sets.

In humans and most other mammals, which are diploid organisms, the somatic cells are diploid cells. However, the sex cells or gametes are haploid, derived from diploid cells via meiosis. This alternation between haploid and diploid forms is crucial for genetic diversity and the formation of new organisms.

Mating types in Basidiomycota

Mushrooms belong to the kingdom Fungi, which does not have distinct sexes. Instead, mating in fungi is controlled by physiological differences defined by mating types. Basidiomycota is a phylum of fungi that includes some of the most iconic fungal species, such as gilled mushrooms, puffballs, and bracket fungi. They inhabit a wide range of ecological niches and play vital roles in carbon cycling and symbiosis with other organisms.

Basidiomycota exhibits a diverse range of mechanisms for sexual reproduction, with multiple mating types being common. Mating types in Basidiomycota are determined by genes that encode two types of homeodomain transcription factors (HD genes) and genes that encode lipopeptide pheromones and pheromone receptors (PR genes). The mating types are further categorized into two mating systems: tetrapolar and bipolar.

In the tetrapolar mating system, two unlinked mating loci, termed A and B (or b and a in some species), control sexual development. The combination of alleles at these loci determines the "specificity" or sexual identity of the individual. Only individuals with different mating types are compatible and can initiate the mating process, which begins with nuclear exchange and migration, leading to the formation of dikaryotic hyphae. Dikaryotic hyphae, under suitable environmental conditions, will develop into a fruiting body containing specialized cells called basidia, where sexual reproduction occurs.

The bipolar mating system, on the other hand, is ruled by a single allelic mating locus, termed either A or b. In Agaricomycotina, bipolar organisms often have multiple alleles for their A mating locus, promoting outcrossing. However, in Ustilaginomycotina and Pucciniomycotina, the b mating locus is predominantly diallelic, reducing the occurrence of outcrossing within these species.

The multiple mating types in Basidiomycota are believed to enhance outbreeding. The mating process involves the reciprocal exchange of diffusible mating pheromones and the interaction of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and the complex patterns of mating-type variation are largely determined by the genetic linkage relationships of the mating pheromone/receptor and homeodomain genes.

Evolution of multicellular fungi

The evolution of multicellularity is considered one of the most significant transitions in the history of life. Multicellular organisms are those that consist of more than one cell, unlike unicellular organisms. All species of animals, land plants, and most fungi are multicellular, along with many algae.

Multicellular life evolved independently and repeatedly in Chloroplastida (green algae and land plants), animals, brown algae, and fungi (chytrids, ascomycetes, and basidiomycetes). True multicellular organisms must be able to regenerate a whole organism from germ cells, such as egg and sperm. Animals have evolved the greatest diversity of cell types in a multicellular body, with 100-150 different types, compared to 10-20 in plants and fungi.

The evolution of multicellular fungi is of particular interest because they followed a different route to other eukaryotic lineages. Comparative genome analyses have been used to develop a model of osmotrophic resource acquisition. This model predicts that when a local resource is immobile, hard to digest, and nutrient-poor, multicellular fungi can outcompete unicellular bacteria due to their ability to transport nutrients via a contiguous cytoplasm. This enables them to continue exploiting resources after local depletion of essential nutrients and to make more efficient use of exoenzymes.

Multicellular fungi also had to overcome several unique challenges arising from their filamentous growth form. These include apical growth, compartmentalization, long-distance mass transport, controlling mutational load, cell-to-cell communication, differentiation, and adhesion.

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