Finally, meiosis takes place in the gametangia singular, gametangium organs, in which gametes of different mating types are generated. At this stage, spores are disseminated into the environment.
Learning Objectives Describe the mechanisms of sexual and asexual reproduction in fungi. Key Points New colonies of fungi can grow from the fragmentation of hyphae. During budding, a bulge forms on the side of the cell; the bud ultimately detaches after the nucleus divides mitotically.
Asexual spores are genetically identical to the parent and may be released either outside or within a special reproductive sac called a sporangium. Adverse environmental conditions often cause sexual reproduction in fungi.
Mycelium can either be homothallic or heterothallic when reproducing sexually. Fungal sexual reproduction includes the following three stages: plasmogamy, karyogamy, and gametangia. Key Terms homothallic : male and female reproductive structures are present in the same plant or fungal mycelium gametangium : an organ or cell in which gametes are produced that is found in many multicellular protists, algae, fungi, and the gametophytes of plants spore : a reproductive particle, usually a single cell, released by a fungus, alga, or plant that may germinate into another sporangium : a case, capsule, or container in which spores are produced by an organism karyogamy : the fusion of two nuclei within a cell plasmogamy : stage of sexual reproduction joining the cytoplasm of two parent mycelia without the fusion of nuclei.
Asexual Reproduction Fungi reproduce asexually by fragmentation, budding, or producing spores. The organism depicted is a Mucor sp. Sexual Reproduction Sexual reproduction introduces genetic variation into a population of fungi. Provided by : Boundless. October 17, Many industrial compounds are byproducts of fungal fermentation.
Fungi are the source of many commercial enzymes and antibiotics. Fungi are unicellular or multicellular thick-cell-walled heterotroph decomposers that eat decaying matter and make tangles of filaments. Fungi are eukaryotes and have a complex cellular organization. As eukaryotes, fungal cells contain a membrane-bound nucleus where the DNA is wrapped around histone proteins. A few types of fungi have structures comparable to bacterial plasmids loops of DNA.
Fungal cells also contain mitochondria and a complex system of internal membranes, including the endoplasmic reticulum and Golgi apparatus.
Unlike plant cells, fungal cells do not have chloroplasts or chlorophyll. Many fungi display bright colors arising from other cellular pigments, ranging from red to green to black. The poisonous Amanita muscaria fly agaric is recognizable by its bright red cap with white patches.
Pigments in fungi are associated with the cell wall. They play a protective role against ultraviolet radiation and can be toxic. The poisonous Amanita muscaria : The poisonous Amanita muscaria is native to temperate and boreal regions of North America. The rigid layers of fungal cell walls contain complex polysaccharides called chitin and glucans. Chitin, also found in the exoskeleton of insects, gives structural strength to the cell walls of fungi. The wall protects the cell from desiccation and predators.
Fungi have plasma membranes similar to other eukaryotes, except that the structure is stabilized by ergosterol: a steroid molecule that replaces the cholesterol found in animal cell membranes. Most members of the kingdom Fungi are nonmotile. The vegetative body of a fungus is a unicellular or multicellular thallus. Dimorphic fungi can change from the unicellular to multicellular state depending on environmental conditions. Unicellular fungi are generally referred to as yeasts. Example of a unicellular fungus : Candida albicans is a yeast cell and the agent of candidiasis and thrush.
This organism has a similar morphology to coccus bacteria; however, yeast is a eukaryotic organism note the nucleus. Most fungi are multicellular organisms.
They display two distinct morphological stages: the vegetative and reproductive. The vegetative stage consists of a tangle of slender thread-like structures called hyphae singular, hypha , whereas the reproductive stage can be more conspicuous. The mass of hyphae is a mycelium. It can grow on a surface, in soil or decaying material, in a liquid, or even on living tissue.
Example of a mycelium of a fungus : The mycelium of the fungus Neotestudina rosati can be pathogenic to humans. The fungus enters through a cut or scrape and develops a mycetoma, a chronic subcutaneous infection. Most fungal hyphae are divided into separate cells by endwalls called septa singular, septum a, c. In most phyla of fungi, tiny holes in the septa allow for the rapid flow of nutrients and small molecules from cell to cell along the hypha. They are described as perforated septa.
The hyphae in bread molds which belong to the Phylum Zygomycota are not separated by septa. Instead, they are formed by large cells containing many nuclei, an arrangement described as coenocytic hyphae b. Fungi thrive in environments that are moist and slightly acidic; they can grow with or without light. A bright field light micrograph of c Phialophora richardsiae shows septa that divide the hyphae. Like animals, fungi are heterotrophs: they use complex organic compounds as a source of carbon, rather than fix carbon dioxide from the atmosphere as do some bacteria and most plants.
In addition, fungi do not fix nitrogen from the atmosphere. Like animals, they must obtain it from their diet. However, unlike most animals, which ingest food and then digest it internally in specialized organs, fungi perform these steps in the reverse order: digestion precedes ingestion.
First, exoenzymes are transported out of the hyphae, where they process nutrients in the environment. Then, the smaller molecules produced by this external digestion are absorbed through the large surface area of the mycelium.
As with animal cells, the polysaccharide of storage is glycogen rather than the starch found in plants. Fungi are mostly saprobes saprophyte is an equivalent term : organisms that derive nutrients from decaying organic matter. They obtain their nutrients from dead or decomposing organic matter, mainly plant material. Fungal exoenzymes are able to break down insoluble polysaccharides, such as the cellulose and lignin of dead wood, into readily-absorbable glucose molecules.
As the pathogen and the host tend to evolve together, different selective pressures apply to these organisms that saprophytic organisms do not encounter.
For these organisms, mating serves as both of mechanism of self versus non-self recognition as well as, in some cases, a means by which to enter the specific host. Increasing host specificity as well as intraspecies recognition are different selective pressures that have shaped the evolution of the mating type loci in these organisms. Human pathogens represent the extreme example within the basidiomycete fungi, where the sexual cycle is not implicated in the infection process.
Generally speaking, saprophytic basidiomycete fungi include mushroom species. Like their ascomycete cousins, these organisms live off dead and decaying organic matter. This group of organisms exemplifies the use of sexual reproduction as a means of increased variation within the fungal kingdom.
Most of the species studied have many alleles at multiple mating type loci, creating much more than two compatible mating types. Sexual reproduction within higher eukaryotes is driven by the selective benefit of creation of variation within the population, but is limited to mating between one of two types of parents, for example male and female. Potentially one of the most well studied mushroom species, Coprinopsis cinerea , also called Coprinus cinereus , is a saprophytic species of mushrooms, known to be an important ecological decomposer.
As in most mushroom systems, mating between compatible mating partners results in the formation of a dikaryon on which mushroom fruiting bodies develop Asante-Owusu et al. There are two groups of mating type genes in Co.
The A mating-type genes encode several genes that can be characterized as providing one of two classes of homeodomain proteins, HD1 or HD2 Asante-Owusu et al. Compatible mating partners bring together different versions of homeodomain proteins that can heterodimerize, generating active transcription factors that lead to sexual development Asante-Owusu et al. The heterodimerization mediated by the N terminus of these homeodomain proteins is an essential component of self versus non-self recognition Asante-Owusu et al.
Different A genes seem to be responsible for clamp cell formation Asante-Owusu et al. In addition to this aspect of mating partner recognition, the B mating locus encodes pheromones and pheromone receptors that also serve in identification of potential mates and govern adjacent cell fusion during mating Asante-Owusu et al. This mushroom species clearly has benefitted from the generation of variability through sexual reproduction.
In nature, this translates into both the increased probability of encountering a compatible mating partner as well as the generation of great genetic variability within a population due to the numerous possibilities of outcrossing. For this organism, sexual reproduction is an essential element of niche formation by increasing fitness through successful mating.
Also of note, genes induced in this species by meiosis are more highly conserved than genes not induced by meiosis in ascomycete fungi like Sa.
Examination of another mushroom species indicates just how many different mating types can be generated with multiallelic mating loci. Another well studied mushroom, Schizophyllum commune , is found in many diverse environments and typically as a wood rot fungus or occasional pathogen of woody species Ohm et al.
While this fungus has recently been found as an opportunist in human infections of immunocompromised hosts, causing, for example, lung infections, and has been associated with soft tissue and nail infections in other animals Chowdhary et al. Like Co. As with the Co. A -dependent regulation results in the upregulation of genes having to do with the cell cycle and the down regulation of genes related to metabolism, while B -dependent genes include those for cell wall and membrane metabolism, stress response, and the redox state of the cell Erdmann et al.
At least 28, different mating types of Sch. Selective pressure on this system has strongly favored increased variation through mating and diversity at the mating type loci to increase the possible mating partners available. While the mushroom species have acquired large numbers of allelic variation within the mating type loci, other basidiomycete fungi have very little variation within these loci across the population, indicating very little out crossing occurs in the population.
Like the ascomycete fungi, the basidiomycete human pathogens tend to avoid mating in clinical populations, while they retain the genetic components required for mating. Other members of this group that mate, do so with other haploid cells from the same meiotic division, and while this strategy does not increase genetic diversity in the population by the mixture of genetic information between two unrelated haploid cells, it does guarantee that the fungus never has to leave the comfort of its host plant to find a compatible mating partner.
Still other Basidiomycetes require a compatible, unrelated mating partner to complete their life cycle and enter their respective host. It is of note that despite the variety of mating strategies, the types of organism that engage in each seems to be relatively consistent. Like their ascomycete cousins, basidiomycete pathogens face a different set of selective pressures than closely related saprophytic organisms due to their interaction with a host.
In a subset of organisms that are phytopathogens, mating is essential for host penetration, meaning meiosis remains an essential element of the lifecycle as the haploid cells capable of mating are the result of meiosis of a diploid cell.
This is in contrast to many of the strategies developed by ascomycete plant pathogens that have ceased to use their ability to mate as it is not required to enter the host plant. However, like the ascomycete mammalian pathogens, basidiomycete fungi that infect human hosts have elusive or absent meiotic and mating pathways despite the genetic components necessary for both. Unlike saprophytic organisms, parasites must also be able to withstand the defenses of the host.
Reactive oxygen species are often produced by plants in response to fungal invasion, which can do damage to fungal genomic integrity. Enzymes involved in eliminating these damaging molecules have been found to be essential virulence factors in many microbial pathogens of plants and in many cases, the invading pathogen uses this defense mechanism against the plant Kim, In these phytopathogens, the occurrence of meiosis following plant infection allows for repair of any DNA damage that may have occurred as a result.
A number of mushroom species have been described as pathogens for a review, see de Mattos-Shipley et al. Additionally, Armillaria mellea , also a plant pathogen, causes Armillaria root rot in many plant species and produces mushrooms around the base of trees it has infected de Mattos-Shipley et al.
Nevertheless, we will not discuss the mating programs and meiosis for these organisms since, for example, Armillaria mellea appears to have a persistent vegetative diploid state in nature Anderson and Ullrich, and the mating system appears to be similar to that of Co. Similarly, M. Accordingly, in the sections that follow, we focus on well-characterized mating system examples from other phytopathogenic fungi, especially smuts, as well as the mostly opportunistic human pathogen, Cryptococcus neoformans.
The fungal tree of life remains a dynamic entity, particularly with the increased availability of molecular and genomic data.
While there is some uncertainly as to the exact placement of many plant pathogens within a fungal phylogenetic tree, the conservation of many aspects of the mating type locus remains indisputable. Ustilago maydis , the causative agent of corn smut, is potentially the most well studied member of the Basidiomycota, and many would argue a better model organism for eukaryotes than Sa.
It has become the standard against which other mating type loci of this group are analyzed see Figures 3 , 4 for a comparison of basidiomycete mating type loci.
In nature, U. When sporidia of opposite mating type recognize each other, they form conjugation tubes and the resulting dikaryon is able to penetrate the host plant. Inside the plant, numerous diploid teliospores are formed inside galls or tumors, giving rise to the characteristic smutted appearance of the plant.
Under suitable conditions, these teliospores germinate, producing haploid sporidia and the cycle continues. Sample tetrapolar mating systems in basidiomycete fungi. While the number of homeodomain proteins may vary across this group, the composition of genetic material at the mating type loci is conserved.
Boxes of the same color represent orthologous components in the different mating types and across species. Sample bipolar mating systems in basidiomycete fungi. While the two mating type loci of these organisms have become physically linked by chromosomal arrangement, the composition of the mating type loci remains similar to that found in tetrapolar systems. The mating type locus in U. The a mating type locus of U. The allele at the a locus is identified as either a1 or a2.
Molecular analysis of the a alleles reveals that the a1 allele is smaller, at 4. The sequences show no homology to each other and are absent in strains of the opposite mating type; i.
Thus, technically they are not true alleles and, as was seen in Sa. The genes mfa1 and mfa2 encode pheromone precursors in their respective mating types and are the only pheromone precursors.
Mutants deleted for mfa1 , for example, are unable to fuse to haploid cells of the opposite mating type Bolker et al. The pheromone receptors are encoded by the pra1 and pra2 genes, and are very similar to the Sa. The receptors are located on the cell surface and bind to a secreted pheromone from a cell of the opposite mating type, resulting in a cellular response leading to preparation for mating Bolker et al.
The b locus of U. The two proteins are either b-East bE or b-West bW , and there have been at least 25 different alleles identified from wild isolates Kronstad and Leong, Deletion of a gene encoding a single homeodomain protein has no effect on phenotype Gillissen et al. The heterodimer acts as a transcription factor for genes necessary to establish the infectious dikaryon and proliferate within the host Kronstad and Leong, Any combination of different alleles from the b locus can cause the dimorphic switch from yeast-like to infectious filamentation and trigger the pathogenic program Schulz et al.
It is possible to form haploid infectious strains simply by introducing homeodomain proteins at the b locus that are capable of forming a heterodimer Kronstad and Leong, While in nature, b proteins derived from the same allele cannot dimerize, synthetic fusions of bE2 and bW2, for example, result in pathogenic development when introduced into haploid strains deleted for the native b locus Romeis et al.
Compatible mating strains recognize each other through the pheromone and pheromone receptor system. For example, after modification, the pheromone Mfa1 secreted by a1 cells is recognized by a pheromone receptor, Pra2, found in the cell membrane of a1 cells. Upon interaction of the pheromone with its receptor, a signaling cascade is activated that leads to phosphorylation of a transcription factor, Prf1 Hartmann et al.
Prf1 binds specifically to pheromone response elements within the a and b mating loci, increasing transcription from both mating type loci and is required for pathogenic development Hartmann et al.
In addition to the activation of Prf1, exposure of compatible mating partners to pheromone results in the growth of conjugation tubes growing toward each other from each haploid cell and eventually fusing Snetselaar and Mims, ; Banuett and Herskowitz, This fusion results in the formation of a dikaryon, and if the two nuclei within this dikaryon also have different alleles at the b mating type loci, filamentation is induced and this structure is able to infect the host corn plants Figure 5.
Mating in Ustilago maydis. A An initial environmental cue, which may be from the plant or involve nutrient limitation, results in the initial phosphorylation of Prf1. B Prf1 binds to a response element in the a mating type loci, resulting in increased expression of the pheromone and pheromone receptor in both types of haploid cells.
C Interaction of the pheromone with the receptor on the cell of opposite mating type results in additional phosphorylation of Prf1. Prf1 phosphorylated by both pathways then binds to response elements within the b mating type locus, leading to increased expression of the homeodomain proteins. Additionally, interaction of pheromone and receptor results in the growth of conjugation tubes from each cell toward each other.
D Creation of a homeodomain heterodimer comprised of bE and bW from different allelles results in the formation of an infection dikaryon. E This dikaryon is able to establish infection within the host, although fusion of the nuclei does not occur during infection until teliospore formation, just prior to release from the infected plant galls.
The b locus seems to be more involved in the development of pathogenicity than the a locus, as diploids that are heterozygous for a but homozygous for b grow in a yeast-like manner and fail to establish infection in host plants Schlesinger et al. Heterozygosity at the a locus is not required for pathogenicity, and diploids homozygous for a but heterozygous for b form similar tumors in host plants as mated haploid strains.
However, in nature, the function of both the a locus and the b locus in a multiallelic incompatibility system functions to limit inbreeding and increase variability within the population Yee and Kronstad, Also, in the synthetic setting of the lab, organisms must be deprived of nutrients, specifically ammonium and possibly phosphorous, in order to see the mating phenotype. Mating is typically observed for U.
Similarly, in nature, mating occurs during appropriate environmental conditions. In this system, mating and sexual reproduction are vital to plant infection. Only synthetically made laboratory haploid strains are able to infect the host corn plant, and in nature, mating and formation of the infectious dikaryon is paramount to establishing infection inside the host, gaining access to the resources inside the host, and proliferating the species. Because of the intrinsic connection between nutrient limitation and induction of mating, it is likely that invasion of the host gives the organism access to nutrients that are needed for survival.
Successfully accessing necessary nutritional components by invading the plant can only be accomplished by being able to recognize a suitable mate, mediated by the mating type loci.
On the other hand, within the host, U. Although the number of different compatible mating strains is much smaller than is observed in the mushrooms, outcrossing does seem to be the preference among this species as well. While the two different haploid cells generated by the germinating teliospore theoretically should be compatible mating partners, mating between these haploids does not appear to occur often in nature.
Examination of two geographically isolated populations of wild U. Because mating is a requirement for host entry in this system, the same potential cost of losing host-specific genetic information is not a driving force in the maintenance of sexual reproduction in this system. While phytopathogenic ascomycete fungi enter their hosts as haploids and the examples reviewed here rarely mate in wild populations, since U.
As such, the benefit of variation within the population gained from outcrossing seems to be a stronger evolutionary pressure. Examination of another closely related species reveals how slight modifications to the maturation process of mating competent cells can further guarantee the recognition of the correct compatible mating partner.
Another smut fungus similar to U. Like some other closely related smuts, the mating type locus is composed of two unlinked genomic regions, a and b , which code for a pheromone and pheromone receptor and homeodomain proteins, respectively. The genetic material within and around these loci shows a high degree of synteny with U.
The b locus exists in at least five different alleles and encodes two subunits of a heterodimeric homeodomain transcription factor Schirawski et al. In contrast to U. These different versions, designated a1, a2, and a3 are idiomorphs. Each idiomorph encodes different pheromones and pheromone receptors. The pheromones for a particular receptor have identical sequence even if they exist in a different allele; that is, the pheromones from a1 and a3 that bind to the receptor from a2 have the same sequence Schirawski et al.
Two of these pheromones, those binding to the receptors of a1 and a2, show a high degree of homology to the corresponding genes in U. This arrangement of two pheromone precursors and one pheromone receptor in each a idiomorph appears to have arisen from a recombination event within the locus itself and serves to increase the number of mating types within the species Schirawski et al. Interestingly enough, despite the narrow host range of the two varieties of Sp.
However, despite the similarity of the genetic material within the mating type loci, SRS is only successfully able to produce teliospores within sorghum and SRZ is only able to do the same in maize. Like other basidiomycete fungi, such as the mushrooms discussed above, more allelic versions of the a locus allow for more mating types and greater variation within the natural populations.
Successful mating only within appropriate hosts guarantees that offspring only carry parental DNA from organisms that are able to establish infection in the host. Recent molecular genomic analysis has placed Ustilago hordei and Ustilago maydis as more distant relatives than their genus name would suggest McTaggart et al.
However, between these two species, the conservation of genetic material within the mating type locus is undeniable. Just as Sa. The elements and arrangement of components of both the a and b mating type loci are highly conserved in their sequences, although the arrangement of genes varies greatly within the group, U.
Like all smuts, the two fungal pathogens share many life cycle features, including a yeast-like stage and an infectious dikaryon arising from the fusion of two haploid cells Bakkeren et al. Unlike the U. In the U. Like the U. Also similar to the other smut, the b locus encodes two homeodomain proteins that during mating dimerize to create a transcription factor to regulate expression of mating-related genes Bakkeren et al.
Interestingly, there is a high degree of sequence similarity between the U. Analyzing the morphological changes that occur upon induction of the mating reaction in U. Another interesting characteristic of the U. While the mating type locus is located within a chromosome that encodes unrelated processes, it is unusually large compared to other smuts and has an accumulation of repetitive DNA and retrotransposons, few of which are found in U.
In addition to the presence of genes for pheromone precursors, pheromone receptors and homeodomain proteins regulating mating and virulence, the U. Because the mating type locus in U. Although U. Previously called Ustilago violaceum and Microbotryum violaceum Day, ; Hood and Antonovics, , ; Hood et al. This fungus is a relatively unique system to study because it acts as a sexually transmitted disease and is capable of changing the gender of its host.
This fungus infects its host and replaces the pollen on anthers with diploid teliospores that are then carried to a new host by bees and other pollinators. Once on the new host, the teliospores germinate, undergo meiosis, and produce haploid sporidia.
If sporidia of compatible mating type encounter each other, they form conjugation tubes and mate, producing dikaryotic hyphae that can grow inside plant tissue.
The infection becomes systemic, eventually leading to the production of teliospores in the place of pollen and the cycle continues Giraud et al. Like U. The mating type loci of Mi. The two mating types of Mi. A2 has two genes encoding pheromone precursors, while A1 contains a single locus Badouin et al. While the two chromosomes seem to be the result of a duplication event by the number of syntenic blocks, extensive rearrangements in the form of inversions have occurred resulting in the gene order currently present Badouin et al.
Before the nature of the genetic material governing compatible mating partners in this organism was fully elucidated, it was discovered that different environmental factors, including low temperature and nutrient availability activated mating type alleles. As regulators of the developmental switch between three pathways of development, vegetative budding, conjugation, and sexual differentiation, mating type allele activity results in different responses to different environmental conditions.
In high temperatures and nutrient levels, cells of this fungus bud vegetatively; however, in correct environmental conditions and upon exposure to the products of cells of opposite mating type presumably pheromones , cells of a single mating type become blocked in G1 and develop conjugation tubes Day, Cells carrying both mating type alleles exposed to similar environmental conditions also could not exit G1 and differentiated into spores Day, Later research also indicated that not only did environmental conditions activate mating, but also governed how the products of mating would act.
The promycelium is the product of teliospore germination in this fungus. Generally speaking, the promycelium contains three cells but at low nutrient and temperature conditions, it may only contain two Hood and Antonovics, An extensive study of promycelia under different environmental conditions revealed different results based on nutrient availability and temperature. After the first meiotic event within the promycelia, the daughter nuclei are separated immediately by septation.
After the second meiotic division, one of the proximal nuclei migrates back into the teliospore; however, based on nutrient availability, the fate of the two distal nuclei can be different Hood and Antonovics, At ideal temperature and nutrient levels, the two distal nuclei are separated by a second septation event, resulting in a three celled promycelium, each of which is uninucleated. At low temperature and nutrient availability, the second septation event does not occur, yielding a two-celled promycelium, with one single nucleated cell and one cell with two nuclei; both of these latter nuclei are of the same mating type, as a result of the two components of the mating type locus being linked Hood and Antonovics, As the number of heterokaryons that can be formed from a two-celled promycelium versus a three-celled promycelium is different, this environmental response allows flexibility of the mating system to either produce more heterokaryons or more infectious units Hood and Antonovics, Because of the complete linkage of the two components of the mating locus, mating between products of the first meiotic division is possible Hood and Antonovics, , which ensures the flexibility of the response in promycelia of different number of cells.
As such, the mating system of Mi. This rapid intratetrad mating allows the organism to form infectious units to gain access to the host plant in response to environmental conditions such as low nutrient availability without having to encounter another cell of different mating type on the surface of the plant.
Outcrossing in this organism seems to be less of an evolutionary driving force; rather continual access to the host plant and avoidance of alleles that would be lethal if given the chance to be expressed in budding haploid cells would here appear to have selected for intratetrad mating as the preferred option Hood and Antonovics, At the opposite extreme, are other basidiomycete fungi that also have highly reorganized mating type loci but are rarely seen to mate in natural settings.
It is of note that most of the examples of this type of organism are human pathogens, as previous evidence from the Ascomycota demonstrates that some of the products of mating can cause strong immune responses, indicating that avoiding mating may be a better strategy for human pathogens.
Upon nitrogen starvation or desiccation, the human fungal pathogen Cryptococcus neoformans undergoes mating or fruiting, both processes involving meiosis Lin et al.
The causative agent of fungal infections in both healthy and immunocompromised individuals, Cr. The infectious particle is either a basidiospore or a desiccated cell, small enough to travel deep within the crevices of the human lung Velagapudi et al. While sexual reproduction for this organism does not occur within the host, it has been observed. Under suitable environmental conditions, fusion between cells of opposite mating type occurs, producing dikaryotic hyphae characteristic of the Basidiomycota Wickes et al.
Several pheromone precursors and pheromone receptor genes have been identified in the genome but unlike model fungal genomes, such as those from U. This may represent yet another transition in the direction of sex chromosomes rather than mating type loci within the genome. While this organism is capable of sexual reproduction, the independent evolution of mating loci within the two mating types has resulted in one mating type of the organism that can establish infection independently of the other.
This phenomenon occurs during haploid fruiting and shares many characteristics of mating, such as the fusion of haploid nuclei and meiosis Lin et al. It may offer further insight into why the majority of clinical isolates are of the same mating type.
Like Pneumocystis carinii , another human fungal pathogen, Cr. In this way, within the host, the organism reaps all the benefits of sexual reproduction, such as repair to DNA damage caused by the host response, without the bother of finding a compatible mating partner. This evolution of the mating type locus represents an extreme example of the accumulation of components of canonical mating type components to the extent that all the benefits of mating can be obtained, while creating a nearly clonal population.
Although the evolution of the mating type locus has not been driven by host interaction, the lack of necessity for metabolically costly mating has shaped the clinical populations.
A resident of the human host, typically associated with dandruff, Malassezia globosa is closely related to Ustilago maydis. This organism and other closely related Malassezia species are part of the normal human epidermal flora but some may become infectious during periods of dense growth that lead to the human symptoms of dandruff and seborrheic dermatitis.
The genome contains components similar to the a and b loci of U. While no sexual cycle has been observed, there are several reasons to believe that this organism is capable of sexual reproduction, including the isolation of strains that appear to be hybrids of other known strains Saunders et al. Sexual reproduction in a human pathogen, if discovered, would be unique to this organism, as others, such as Ca. In contrast to the human pathogens that retain the components necessary for mating but seem to avoid outcrossing, other basidiomycete fungi, particularly the mushrooms have evolved a multitude of variations at the mating type loci for the purpose of creating diversity within the mating population.
Sexual reproduction, particularly in higher eukaryotes, is the only means of producing additional generations and allows for allelic shuffling between the mating pair. Although this increase in variation seems like it would be favored by natural selection, examination of organisms with sexual and asexual forms of reproduction indicates that the favorability increased variation rendered by sexual reproduction must be weighed against the cost of reproduction, both in the context of cost to the individual organism and, for those organisms that are pathogens, ability to avoid the immune response of a potential host.
Within the Ascomycota, although many species readily mate in the lab, mating in wild type populations is much less common. Although all members of this group seem to possess the genetic information comprising a mating type locus, few regularly engage in sexual reproduction.
In saprophytic species like Sa. However, as it can be demonstrated in the lab setting that nutrient limitation can induce meiosis and sporulation, as in the case of Sa.
Losing the genetic material at the mating type loci would equate to losing the ability to repair DNA through recombination during mating. The importance of maintaining the components for sexual reproduction is even more evident in human pathogens like Ca. These organisms only undergo a parasexual cycle, so while they do not outcross often, genetic recombination does occur.
Most clinical isolates are white, while mating competent strains are opaque. The switch between these types is governed by the mating type loci. Because the product of mating, the haploid yeast cells, evoke the strongest immune response from the human host, this organism gets the repair mechanism of mating without expending the cost of potentially alerting the immune system to its presence.
Other pathogenic species, particularly plant pathogens, also have developed alternate methods of using the genetic material involved in mating or not using it at all. The most adaptive example is that of Fusarium which uses the pheromone receptors to detect the presence of potential plant hosts. Unlike the Ascomycota presented here, all of the Basidiomycota discussed reproduce sexually, whether they are saprophytic or pathogenic. Interestingly, as seen with the Ascomycota, human pathogens like Cr.
Also, as is the case for the sac fungi, basidiomycete fungi mate in the lab when exposed to potential sources of DNA damage, such as nutrient deprivation. Although these species engage in sexual reproduction, the extent to which outcrossing occurs is more inconsistent within the group. Such is also the case for U. The two latter fungal pathogens have each evolved individual strategies for increasing the probability of successful mating, such as chromosomal rearrangements returning to a bipolar mating system U.
In any of the three cases, mating is essential for the organism to enter a host and complete its respective lifecycle. For other organisms, outcrossing has become less essential although mating remains an integral step in the completion of the lifecycle.
For example, Mi. Like the ascomycete fungus Ca. In this way, they increase the probability of any two haploid cells being compatible for mating and increase the diversity of the species. It is of note that these organisms are generally saprophytic and are not subject to the selective pressures of co-evolving within a plant or mammalian host. In the Ascomycota, saprophytic organisms rarely mate, while in the Basidiomycota, saprophytic organisms mate more than pathogenic organisms and create extensive species diversity through differences in the mating type loci.
Pathogenic ascomycete fungi rarely mate because of the possibility of evoking immune response from the host, while most plant pathogenic basidiomycete fungi must mate in order to access their hosts.
Because the mating type loci are maintained in all of these dikaryotic fungi, their retention undoubtedly provides a fitness advantage over those organisms who have lost this genetic information. The most plausible reason for maintaining the ability to mate seems to be repairing DNA damage caused by a variety of conditions, through recombination that occurs during meiosis. In the evolutionary arms race, for mammalian pathogenic species, the use of the mating type loci may have waned in favor of avoiding immune response.
However, throughout the course of co-evolution, while the organisms reproduce sexually at a much lower frequency than other members of the dikaryotic fungi, maintenance of the mating type loci has been favored by selection or it would have disappeared in the organisms that rarely use it. Of course, there are exceptions such as P. For plant pathogens, the mating type loci for ascomycete fungi have basically become vestigial genetic information in some species, either not used or repurposed; in contrast, for basidiomycete fungi, sexual reproduction is an essential element of plant pathogen host penetration.
However, in all cases, the maintenance of mating type loci in dikaryotic fungi is associated with their fitness relative to organisms that lose this genetic information. If the selective advantage of maintaining a meiotic pathway were purely for creating variation, this strategy allowing for meiosis without increasing variation would not be maintained with this group of fungi.
Rather, it seems that increase in variation was a fortunate byproduct of a system originally evolved to handle stressful environmental conditions. Not all members of either group have been studied extensively and much remains to be learned about the function of mating type loci in the remaining dikaryotic fungi. The organisms included in this review are by no means a complete list of all the interesting and sometimes elusive strategies of sexual reproduction within dikaryotic fungi.
Analysis of these organisms does provide insight into the complexity of sexual reproduction in all eukaryotes, especially as it is related to ecological niche. Nearly all organisms reviewed contain at least part of the mating type loci, even those with the most frugal genomes, indicating the ancestral state as well as the importance of mating in the evolutionary history of these organisms.
Strong evidence suggests that mating and nutrient deprivation are closely linked, potentially as a way to survive adverse environmental conditions. Examples of increased variation as well as virtually clonal populations indicate that mating and sexual reproduction have not always been used for the same purpose within this group of fungi. Thus, much remains to be learned about the function of sex in eukaryotes as a whole.
The authors declare that this manuscript follows the Ethical Responsibilities of Authors, as indicated in the Instructions to Authors including not being previously published or simultaneously submitted elsewhere, and consent of all authors. Both authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. RW and MP developed the concept of the review. RW did the bulk of the initial literature research, figure production, and writing.
MP helped with overall organization and editing to produce the final product. The contents of this work are solely the responsibility of the authors and do not represent the official views of the NIH. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Deborah Yoder-Himes, Dr. David J. Schultz, Dr. James E. Graham, and Dr. Carolyn M. Klinge, all from the University of Louisville, for their invaluable insight into creation of this document. Finally, the authors thank the three reviewers from the journal that provided constructive criticisms that ultimately led to a much-improved finished product.
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