Mating in fungi
Fungi are a diverse group of organisms that employ a huge variety of reproductive strategies, ranging from fully asexual to almost exclusively sexual species.[1] Most species can reproduce both sexually and asexually, alternating between haploid and diploid forms. This contrasts with most multicellular eukaryotes such as mammals, where the adults are usually diploid and produce haploid gametes which combine to form the next generation. In fungi, both haploid and diploid forms can reproduce – haploid individuals can undergo asexual reproduction while diploid forms can produce gametes that combine to give rise to the next generation.[2]
Mating in fungi is a complex process governed by mating types. Research on fungal mating has focused on several model species with different behaviour.[3][4] Not all fungi reproduce sexually and many that do are isogamous; thus, for many members of the fungal kingdom, the terms "male" and "female" do not apply. Homothallic species are able to mate with themselves, while in heterothallic species only isolates of opposite mating types can mate.
Mating between isogamous fungi may consist only of a transfer of a nucleus from one cell to another. Vegetative incompatibility within species often prevents a fungal isolate from mating with another isolate. Isolates of the same incompatibility group do not mate or mating does not lead to successful offspring. High variation has been reported including same-chemotype mating, sporophyte to gametophyte mating and biparental transfer of mitochondria.
-
Fungi within Zygomycota form progametangia with suspensors during mating
-
Fungi within Ascomycota form ascogonium and antheridium with trichogyne bridge
-
Typical mating fusion of two compatible monokaryons in Basidiomycota
Mating in Zygomycota
A
Mating in Ascomycota
As it approaches a mate, a
Neurospora crassa
Neurospora crassa is a type of red bread mold of the phylum Ascomycota. N. crassa is used as a model organism because it is easy to grow and has a haploid life cycle: this makes genetic analysis simple, since recessive traits will show up in the offspring. Analysis of genetic recombination is facilitated by the ordered arrangement of the products of meiosis within a sac-like structure called an ascus (pl. asci). In its natural environment, N. crassa lives mainly in tropical and sub-tropical regions. It often can be found growing on dead plant matter after fires.
Neurospora was used by
The subsequent steps following fusion of A and a haploid cells have been outlined by Fincham and Day.[9] and Wagner and Mitchell.[10] After fusion of the cells, the further fusion of their nuclei is delayed. Instead, a nucleus from the fertilizing cell and a nucleus from the ascogonium become associated and begin to divide synchronously. The products of these nuclear divisions (still in pairs of unlike mating type, i.e. A/a) migrate into numerous ascogenous hyphae, which then begin to grow out of the ascogonium. Each of these ascogenous hyphae bends to form a hook (or crozier) at its tip and the A and a pair of haploid nuclei within the crozier divide synchronously. Next, septa form to divide the crozier into three cells. The central cell in the curve of the hook contains one A and one a nucleus (see Figure). This binuclear cell initiates ascus formation and is called an “ascus-initial” cell. Next the two uninucleate cells on either side of the first ascus-forming cell fuse with each other to form a binucleate cell that can grow to form a further crozier that can then form its own ascus-initial cell. This process can then be repeated multiple times.
After formation of the ascus-initial cell, the A and a nuclei fuse with each other to form a diploid nucleus (see Figure). This nucleus is the only diploid nucleus in the entire life cycle of N. crassa. The diploid nucleus has 14 chromosomes formed from the two fused haploid nuclei that had 7 chromosomes each. Formation of the diploid nucleus is immediately followed by meiosis. The two sequential divisions of meiosis lead to four haploid nuclei, two of the A mating type and two of the a mating type. One further mitotic division leads to four A and four a nucleus in each ascus. Meiosis is an essential part of the life cycle of all sexually reproducing organisms, and in its main features, meiosis in N. crassa seems typical of meiosis generally.
As the above events are occurring, the mycelial sheath that had enveloped the ascogonium develops as the wall of the perithecium becomes impregnated with melanin, and blackens. The mature perithecium has a flask-shaped structure.
A mature perithecium may contain as many as 300 asci, each derived from identical fusion diploid nuclei. Ordinarily, in nature, when the perithecia mature the ascospores are ejected rather violently into the air. These ascospores are heat resistant and, in the lab, require heating at 60 °C for 30 minutes to induce germination. For normal strains, the entire sexual cycle takes 10 to 15 days. In a mature ascus containing eight ascospores, pairs of adjacent spores are identical in genetic constitution, since the last division is mitotic, and since the ascospores are contained in the ascus sac that holds them in a definite order determined by the direction of nuclear segregations during meiosis. Since the four primary products are also arranged in sequence, a first division segregation pattern of genetic markers can be distinguished from a second division segregation pattern.
Benefit of mating type in N. crassa
That mating in N. crassa can only occur between strains of different mating type suggests that some degree of outcrossing is favored by natural selection. In haploid multicellular fungi, such as N. crassa, meiosis occurring in the brief diploid stage is one of their most complex processes. The haploid multicellular vegetative stage, although physically much larger than the diploid stage, characteristically has a simple modular construction with little differentiation. In N. crassa, recessive mutations affecting the diploid stage of the life cycle are quite frequent in natural populations.[11] These mutations, when homozygous in the diploid stage, often cause spores to have maturation defects or to produce barren fruiting bodies with few ascospores (sexual spores). The majority of these homozygous mutations cause abnormal meiosis (e.g. disturbed chromosome pairing or disturbed pachytene or diplotene).[12] The number of genes affecting the diploid stage was estimated to be at least 435[11] (about 4% of the total number of 9,730 genes). Thus, outcrossing, promoted by the necessity for union of opposite mating types, likely provides the benefit of masking recessive mutations that would otherwise be deleterious to sexual spore formation (see Complementation (genetics)).
Saccharomyces cerevisiae
Katz Ezov et al.[15] presented evidence that in natural S. cerevisiae populations clonal reproduction and a type of “self-fertilization” (in the form of intratetrad mating) predominate. Ruderfer et al.[14] analyzed the ancestry of natural S. cerevisiae strains and concluded that outcrossing occurs only about once every 50,000 cell divisions. Thus, although S. cerevisiae is heterothallic, it appears that, in nature, mating is most often between closely related yeast cells. The relative rarity in nature of meiotic events that result from outcrossing suggests that the possible long-term benefits of outcrossing (e.g. generation of genetic diversity) are unlikely to be sufficient for generally maintaining sex from one generation to the next.[citation needed] Instead, a short-term benefit, such as meiotic recombinational repair of DNA damages caused by stressful conditions such as starvation, may be the key to the maintenance of sex in S. cerevisiae.[16] Alternatively, recessive deleterious mutations accumulate during the diploid expansion phase, and are purged during selfing: this purging has been termed "genome renewal" and provides an advantage of sex that does not depend on outcrossing.[17][18]
Candida albicans
Candida albicans is a diploid fungus that grows both as a yeast and as a filament. C. albicans is the most common fungal pathogen in humans. It causes both debilitating mucosal infections and potentially life-threatening systemic infections. C. albicans has maintained an elaborate, but largely hidden, mating apparatus.[19] Johnson suggested that mating strategies may allow C. albicans to survive in the hostile environment of a mammalian host. In order to mate C. albicans needs to switch from white to opaque cells. The latter are more efficient in mating and referred to as the mating competent cells of C. albicans. Mating in C. albicans is termed a parasexual cycle since meiosis is still not observed in C. albicans.[20][21]
Mating type
A picture of the mating type mechanism has begun to emerge from studies of particular fungi such as S. cerevisiae. The mating type genes are located in homeobox and encode enzymes for production of pheromones and pheromone receptors. Sexual reproduction thereby depends on pheromones produced from variant alleles of the same gene. Since sexual reproduction takes place in haploid organisms, it cannot proceed until complementary genes are provided by a suitable partner through cell or hyphal fusion. The number of mating types depends on the number of genes and the number of alleles for each.
Depending on the species, sexual reproduction takes place through gametes or hyphal fusion. When a receptor on one haploid detects a pheromone from a complementary mating type, it approaches the source through chemotropic growth or chemotactic movement if it is a gamete.
Mating in Basidiomycota
Some of the species within
Tetrapolar and bipolar mating system
Heterothallism is the most common mating system in Basidiomycota and in Agaricomycotina (the mushroom-forming fungi) about 90% of the species are heterothallic.[22] The tetrapolar type of mating system is ruled by two unlinked mating loci termed A and B (in Agaricomycotina) or b and a (in Ustilaginomycotina and Pucciniomycotina), both of which can be multiallelic. The combination of A and B (or b and a) alleles, termed mating type, determine the "specificity" or sexual identity of the individual harboring them. Only individuals with different mating types are compatible with each other and therefore able to start the mating event.
A successful mating interaction begins with nuclear exchange and nuclear migration resulting in the formation of
Examples of tetrapolar organisms are the smuts
It is believed that multi-allelic systems favor outcrossing in Basidiomycota. For example, in the case of U. maydis, which bears more than 25 b but only 2 a mating types, an individual has an approximately 50% chance to encounter a compatible mate in nature.[26] However, species such as C. cinerea, which has more than 240 A and B mating types, each, and S. commune, which has more than 339 A mating types and 64 B mating types, approach close to 100% chance of encountering a compatible partner in nature, due to the huge number of mating types generated by these systems.[27]
In contrast, bipolar mating systems are ruled by a single allelic mating locus, termed either A or b. In Agaricomycotina, bipolar organisms mostly have multiple alleles for their A mating locus; however, in Ustilaginomycotina and Pucciniomycotina, the b mating locus is predominantly diallelic, which reduces the occurrence of outcrossing within these species.[23] Bipolarity likely arose via one of two potential routes:
- During evolution the B or a locus lost functionality in determining mating type, as has occurred in the mushroom Coprinellus disseminatus.[28]
- Both mating loci have become physically linked such that they now act as a single locus; this has occurred in the smut plant pathogen U. hordei[29] and in the human pathogen Cryptococcus neoformans.[30] Virulence success in these two pathogens is highly associated with mating and their mating type locus.[26]
Other bipolar species include the white rot fungus
The A and B or b and a mating loci
In the B or a locus there are linked genes that code for
The A or b mating locus contains genes that code for two types of homeodomain transcription factor proteins, usually tightly linked, that are homologues to the Saccharomyces cerevisiae mating proteins MATα2 and MATa1. In Agaricomycotina the two types of homeodomain transcription factors are termed HD1 and HD2; so the HD1 and HD2 proteins from an individual interacts with the HD2 and HD1 proteins from the other partner, respectively, generating heterodimers able to activate the A transcriptional regulated pathway, which involves formation of clamp cells, coordinated
Homothallism
Homothallic species may likely have evolved from heterothallic ancestors (Lin and Heitman 2007). In Basidiomycota homothallism is not very common and in Agaricomycotina it is estimated that only 10% of species have homothallic mating behavior.
Among the 250 known species of aspergilli, about 36% have an identified sexual state[37] Among those Aspergillus species that exhibit a sexual cycle the overwhelming majority in nature are homothallic (self-fertilizing).[37] Selfing in the homothallic fungus Aspergillus nidulans involves activation of the same mating pathways characteristic of sex in outcrossing species, i.e. self-fertilization does not bypass required pathways for outcrossing sex but instead requires activation of these pathways within a single individual.[38] Fusion of haploid nuclei occurs within reproductive structures termed cleistothecia, in which the diploid zygote undergoes meiotic divisions to yield haploid ascospores.
See also
- Mating of yeast
- Mating type
- Mating-type region
- Neurospora crassa
- Dioecy § In mycology
- Fungus § Reproduction
References
- PMID 27619703.
- PMID 29619017.
- PMID 15012495.
- PMID 19898490.
- ISBN 978-0-393-42865-0.
- PMID 15020400.
- JSTOR 2437339.
- PMID 1356883.
- ^ Fincham J RS, Day PR (1963). Fungal Genetics. Blackwell Scientific Publications, Oxford, UK. ASIN B000W851KO
- ^ Wagner RP, Mitchell HK. (1964). Genetics and Metabolism. John Wiley and Sons, Inc., New York ASIN B00BXTC5BO
- ^ PMID 2933298.
- PMID 1427061.
- PMID 3070323.
- ^ S2CID 783720.
- PMID 20002587.
- ISBN 978-0306472619
- S2CID 11989104.
- PMID 21888925.
- S2CID 1826178.
- PMID 15910278.
- S2CID 13859192.
- ^ a b James, Timothy (2007). "Analysis of mating type locus organization and synteny in mushroom fungi: Beyond model species". In Heitman, J.; Kronstad, J.W.; Taylor, J.W.; Casselton, L.A. (eds.). Sex in Fungi: Molecular Determination and Evolutionary Implications. Washington, DC: ASM Press. pp. 317–331.
- ^ PMID 8844149.
- PMID 1967554.
- PMID 20190072.
- ^ PMID 18935978.
- ^ a b Casselton, L.A.; Kües, U. (2007). "The origin of multiple mating types in the model mushrooms Coprinopsis cinerea and Schizophyllum commune". In Heitman, J.; Kronstad, J.W.; Taylor, J.W.; Casselton, L.A. (eds.). Sex in Fungi: Molecular determination and evolutionary implications. Washington, DC: ASM Press. pp. 283–300.
- PMID 16461425.
- PMID 7913746.
- PMID 12455690.
- PMID 21131435.
- S2CID 25670803.
- ^ PMID 11418220.
- PMID 1310895.
- ^ Lin, X.; Heitman, J. (2007). "Mechanisms of Homothallism in Fungi and Transitions between Heterothallism and Homothallism". In J. Heitman; J. W. Kronstad; J. W. Taylor; L. A. Casselton (eds.). Sex in Fungi: Molecular Determination and Evolutionary Implications. Washington DC: ASM Press. pp. 35–57.
- S2CID 36453261.
- ^ PMID 22091779.
- PMID 17669651.