Variation in a population may arise following sexual reproduction. Two compatible isolates of the same fungus may initiate reproduction, and the basic process is remarkably similar in all fungi. The isolates first recognise each other and potentially conjugant regions are induced, probably because of the release and recognition of specific hormones. Growth of one or both towards the other, and contact between the two isolates is followed by fusion of the cells (plasmogamy). Nuclei from one pass to the other thallus. Nuclei fuse (karyogamy), perhaps multiply and spread, within the second, before the reproductive units are formed. The details of sexual structures, and process and location of plasmogamy, karyogamy and meiosis differ between fungal taxa.
How do fungi recognise one another, and once aware, get together? Sexual compatibility is determined by mating systems. Various patterns are found. A few fungi are homothallic, and are thus capable of forming sexual structures within a single thallus. Most fungi appear to be heterothallic, requiring compatible mating types on different thalli for sexual reproduction to be initiated.
Fungi release minute quantities of specific compounds that indicate their specific identity. The compounds, commonly called hormones, are genetically determined. When one fungus recognises a hormone in its environment, it will respond by developing a structure that grows towards the source of the hormone. Similarly, if the hormone producer recognises the hormone produced by the recipient isolate, then it will respond by the formation of a structure that grows towards the hormone producer. This interaction is said to be compatible if the two extensions meet, and fuse. LINK
Sex hormones have been characterised in the genus Allomyces, some Mucorales and Ascomycota. The specific processes involved in fusion between compatible thalli, however, are unclear.
Following fusion of thalli (plasmogamy), the nucleus of one thallus is tranferred to the second, where the haploid nuclei fuse (karyogamy). While fusion between haploid and dikaryotic or diploid hyphae has been recorded, the interaction between different types of nuclei is commonly incompatible.
Incompatibility between two separate thalli indicates genetic separation. Incompatible interactions can take place prior to, at or following fusion (see cartoon above). While induced hyphae of two different thalli may grow towards one another, the cells need not meet. The cells may meet and one or both cells may immediately die. Fusion incompatibility prevents vegetative fusion in haploid filamentous fungi. Incompatibility following fusion or post-fusion incompatibility is far more common within species. Two strains with different genetic constitution may fuse. However, death of the connected and adjacent compartments following fusion indicate a strong allelic incompatibility.
In a few fungal species e.g. Thanatophoris cumcumeris (and Rhizoctonia solani) incompatibility is used to indicate genetic differences within one species. LINK
Vegetative fusion (anastomosis) is common between hyphae of germinating spores of one genetic type. It leads to the immediate formation of a thallus with a single karyotype. This is referred to as vegetative compatibility.
In addition, hyphae of compatible fungi may anastomose during growth, and if the nucleus from one is passed to the other, may form a dikaryon. If these nuclei are genetically different, the resultant organism is a heterokaryon, containing two nuclei in each compartment, each being haploid.
Fusion between colonies of different genetic origin is less common. Fusion of cytoplasm may lead to two deleterious consequences: acquisition of unwanted genetic material such as viruses and plasmids, and pirate nuclei with the capacity to replace the existing nucleus.
It is tempting to equate sexual compatibility with sex. This is incorrect. Some Ascomycota which establish colonies from haploid spores may form protoperithecia and conidia. The fertilisation of the protoperithecia can only take place through contact from conidia from a complementary mating type. Sexual compatibility ensures outcrossing.
Further, it is tempting to assume that two different isolates are needed for formation of the sexual spore. Homothallic fungi do not. In homothallic fungi, the individual mycelium mates with itself and produces viable offspring. The thallus produces sex organs of both types, and passes through the sexual process forming viable zygotes. Homothallism enables isolated fungi to go through the sexual process where no compatible mycelia are present. Homothallic isolates are particularly common in isolates of fungi maintained in the laboratory. Particularly successful genotypes may be sustained by homothallism in a sexually reproducing population.
The fungi have a variety of compatibility genes involved in outcrossing. LINK The simplest system is where a single locus has two alleles, leading to a sexual interaction where both alleles are involved. Where only one type of allele is present, the interaction is incompatible.
If compatibility is determined at one locus, the resultant mating system is known as bipolar. That is, in the diploid, the mating locus has two different compatible alleles at the locus. Usually, any two different alleles will result in a compatible interaction. Single locus, two allele systems are found in some flagellated fungi, Zygomycota and Ascomycota, as well as the rusts and smut fungi, and some other Basidiomycota.
In the remaining Basidiomycota, mating is more complex. Compatibility is determined by two loci or linked regions, each of which may have many different alleles. The mating system is called tetrapolar if two loci determine compatibility. Here, a compatible interaction requires different alleles at each of the two loci.
The consequence of multiple alleles at one locus is that in a mixed population, almost any mating will produce a compatible interaction. In comparison, self-mating results in a reduced level of compatibility. Remember that if only two alleles at one locus, 50% of all potential interactions are compatible. If selfing with a tetrapolar cross, then 25% of crosses will be compatible. However, most crosses will be compatible with outcrossing in a tetrapolar cross.
Tetrapolar interactions are more complicated. This is because the interaction may be staged: one locus determines whether the hyphae combine, the second determines whether the organism produces a sexual structure. For a dikaryon to be fertile, the alleles at each locus must be different.
These combinations seem odd, as they are likely to lead to difficulties in successful matings. Some of these fungi form secondarily homothallic mycelia in apparently heterothallic mycelia. Each spore may contain a pair of compatible nuclei. Indeed, some mating type alleles are "silent" in the genome of some fungi, resulting in successful mating because the mating type has switched.
Successful fusion of nuclei is followed by meiosis.
Compatible fusions have other consequences. The fusion of thalli of different genetic background will inevitably also involve the transfer of some cytoplasm. Most of the functional genes are carried in the nucleus. Thus the basic development and most functions of the cell are determined by the movement of nuclei following compatible interactions.
Nucleic acid is carried in the nucleus of the cell and the nuclear region of the mitochondria, plasmids in the cell cytoplasm and the mitochondria, and in viruses LINK (note most viruses are constructed from RNA, but we will treat DNA and RNA together here). Whatever the source, the nucleic acid can influence the function of the compartment carrying the nucleic acid.
Most mitochondria have genes for basic functions of the mitochondria, including ribosomal subunits, tRNAs, and some enzymes. Some further genes are shared between the host nucleus and the mitochondria, and these genes vary within the fungi. The genome also contains open reading frames which appear in some cases to be mobile and thus transferrable between different isolates. The mobile elements may lead to recombination when mitochondria of different strains meet in a compartment.
Transfer of mitochondria from one thallus to another is uncommon during compatible interactions. Transfer is rarely found outside the compartment where the nuclei first meet. The nucleus is transferred, but a barrier to cytoplasmic transfer seems effective. Transfer of viruses is more common, and the mechanism which enables transfer of viruses but not mitochondria is unknown. We know even less about the transfer of mobile genetic elements.
Mitochondrial genomes are remarkably diverse. Some are found in a linear form, others circular. Both forms may be found in one mitochondrion. Functionally, the genome is plastic and recombination between mitochondria from different parents has been observed in Aspergillus nidulans. Thus cytoplasmic inheritance may include characteristics of either or both parents or a recombination of each in dikaryotic fungi.
While some forms of extranuclear nucleic acid are standard prokaryote plasmids, others appear to be viruses, with their own polymerases. Plasmids consist of DNA and some have interesting functions. One in Fusarium solani appears to determine host specificity of the plant pathogenic fungus.
Most viruses have double stranded RNA and form encapsulated particles. They are commonly found in cytoplasm of the cell or mitochondria. While most viruses have no detectable effect on their host, a few are locally important. A putative virus determines virulence in the plant pathogen Ceratocystis ulmi. A virus is associated with toxin production in the killer strain of yeast. A different virus enables an endophyte to enhance the capaciy of its host plant to tolerate high temperatures.
The variation induced by extrachromosomal inheritance is further complicated by the insertion of some of these genomes into the chromosomes of the nucleus or nuclear region of the mitochondrion, either disrupting essential genes or providing a transferable gene. One of the challenges of mycologists is to determine how fungi, with extraneous DNA, manage to reduce the losses associated with their presence.
Compatibility determines the interaction between different thalli. Two parts of the same fungus may separate and fuse over time. Clearly, the fungus is the same organism, and only mutations in the genes for recognition and fusion will prevent the continuation of compatible fusions (anastomoses).
The compatibility factors also determine the potential for sexual reproduction. Interestingly, the more complex the process of compatibility the more likely that different isolates of the same species will form a sexual structure.
Compatibility also involves processes that we do not yet understand. For instance, the process of wall disintegration during fusion, and the prevention of transfer of cytoplasm, are clearly under tight cellular control. How fungi control these functions remains to be clarified.
Burnett J. (2003) Fungal Populations and Species. OUP.
Davis R.H. (2000) Neurospora. QUP.
Elliott CG (1994) Reproduction in Fungi: Genetical and physiological aspects. Chapman Hall.
Rhizoctonia solani Kuhn is a species of basidiomycetous fungi known to include plant pathogens, saprotrophs, and mycorrhizal symbionts of orchids. The teleomorph of the fungus, Thanatephorus cucumeris (Frank) Donk, is rarely observed in culture, so the anamorph is the more widely used name. The fungus is widespread, and of considerable economic importance.
R. solani is characterised by some brown pigmentation, branching near distal septa of cells in young hyphae, constriction of hyphae and formation of a septum a short distance from the branch point, a dolipore septa, and multinucleate cells. The fungus lacks asexual spores, and it commonly forms sclerotia in culture, and may form barrel-shaped cells in plant tissue. Varieties of fungi within the species appear to have different biological properties. The practical method of identifying R. solani relies on the variety of compatibility groupings within the species.
R. solani is divided into at least 13 anastomosis groups (AGs). Within each anastomosis group, vegetatively compatible interactions take place. When two compatible fungi are placed together on agar, one of two reactions may be observed: the hyphae of each fuse (C3) and the different thalli become indistinguishable, or the hyphae fuse and the compartments surrounding the fusion site loose their contents after a short period (C2). When paired with isolates from different compatibility groups, the result is a rejection reaction or no interaction. Some fungi are "bridging" types, meaning they may anastomose with more than one AG.
The concept of anastomosis groups may be confusing in this fungus, due to the behaviour of the multiple nuclei, usually four to six, in the compartments. The nuclei may be from different backgrounds. Occasionally, one or more of the nuclei are not passed into the new compartment at a mitotic division. Thus on agar, segments may form which do not anastomose with the parent from which they were subcultured. That is, anastomosis breaks down within one anastomosis group.
The AGs in Rhizoctonia solani have a predictable biology. For instance, the recently described AG 12 is only known to form mycorrhizas with orchids, and has only been found in Australia so far. AG 8 is a serious pathogen of wheat in Australia. AG 1 is a pathogen of a range of crop plants, including corn, rice and soybean. AG 6 includes weak pathogens, saprophytes and mycorrhizal fungi.